Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations

Tobler, Michael; Plath, Martin; Riesch, Rüdiger; Schlupp, Ingo; Grasse, Anna V.; Munimanda, Gopi K.; Setzer, Claudia; Penn, Dustin J.; Moodley, Yoshan

doi:10.1111/jeb.12370

Cited by 35 publications

(51 citation statements)

References 80 publications

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“…1829 alleles in the human MHC II DRB gene; de Bakker & Raychaudhuri ), and its polymorphism is considered an adaptive trait maintained by balancing selection (Oliver & Piertney ; Tobler et al . ).…”

Section: Introductionmentioning

confidence: 97%

Balancing selection and genetic drift create unusual patterns of MHCIIβ variation in Galápagos mockingbirds

et al. 2016

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The extracellular subunit of the major histocompatibility complex MHCIIβ plays an important role in the recognition of pathogens and the initiation of the adaptive immune response of vertebrates. It is widely accepted that pathogen-mediated selection in combination with neutral micro-evolutionary forces (e.g. genetic drift) shape the diversity of MHCIIβ, but it has proved difficult to determine the relative effects of these forces. We evaluated the effect of genetic drift and balancing selection on MHCIIβ diversity in 12 small populations of Galápagos mockingbirds belonging to four different species, and one larger population of the Northern mockingbird from the continental USA. After genotyping MHCIIβ loci by high-throughput sequencing, we applied a correlational approach to explore the relationships between MHCIIβ diversity and population size by proxy of island size. As expected when drift predominates, we found a positive effect of population size on the number of MHCIIβ alleles present in a population. However, the number of MHCIIβ alleles per individual and number of supertypes were not correlated with population size. This discrepancy points to an interesting feature of MHCIIβ diversity dynamics: some levels of diversity might be shaped by genetic drift while others are independent and possibly maintained by balancing selection.

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Section: Introductionmentioning

confidence: 97%

Balancing selection and genetic drift create unusual patterns of MHCIIβ variation in Galápagos mockingbirds

et al. 2016

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“…As such, a range of classic immunological candidate genes have been implicated, including the major histocompatibility complex (MHC) (Piertney & Oliver ; Tobler et al . ), interferon gamma (IFNG) (Coltman et al . ; Stear et al .…”

Section: Introductionmentioning

confidence: 99%

Genome‐wide association and genome partitioning reveal novel genomic regions underlying variation in gastrointestinal nematode burden in a wild bird

et al. 2015

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Identifying the genetic architecture underlying complex phenotypes is a notoriously difficult problem that often impedes progress in understanding adaptive eco-evolutionary processes in natural populations. Host-parasite interactions are fundamentally important drivers of evolutionary processes, but a lack of understanding of the genes involved in the host's response to chronic parasite insult makes it particularly difficult to understand the mechanisms of host life history trade-offs and the adaptive dynamics involved. Here, we examine the genetic basis of gastrointestinal nematode (Trichostrongylus tenuis) burden in 695 red grouse (Lagopus lagopus scotica) individuals genotyped at 384 genome-wide SNPs. We first use genome-wide association to identify individual SNPs associated with nematode burden. We then partition genome-wide heritability to identify chromosomes with greater heritability than expected from gene content, due to harbouring a multitude of additive SNPs with individually undetectable effects. We identified five SNPs on five chromosomes that accounted for differences of up to 556 worms per bird, but together explained at best 4.9% of the phenotypic variance. These SNPs were closely linked to genes representing a range of physiological processes including the immune system, protein degradation and energy metabolism. Genome partitioning indicated genome-wide heritability of up to 29% and three chromosomes with excess heritability of up to 4.3% (total 8.9%). These results implicate SNPs and novel genomic regions underlying nematode burden in this system and suggest that this phenotype is somewhere between being based on few large-effect genes (oligogenic) and based on a large number of genes with small individual but large combined effects (polygenic).

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“…However, none of these studies demonstrate explicitly variations in pathogen communities across populations (but see Charbonnel and Pemberton 2005 and Tobler et al. 2014). …”

Section: Introductionmentioning

confidence: 99%

Genetic structure in insular and mainland populations of house sparrows (Passer domesticus) and their hemosporidian parasites

Bichet

Moodley

Penn

et al. 2015

Ecology and Evolution

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Small and isolated populations usually exhibit low levels of genetic variability, and thus, they are expected to have a lower capacity to adapt to changes in environmental conditions, such as exposure to pathogens and parasites. Comparing the genetic variability of selectively neutral versus functional loci allows one to assess the evolutionary history of populations and their future evolutionary potential. The genes of the major histocompatibility complex (MHC) control immune recognition of parasites, and their unusually high diversity is genes which is likely driven by parasite-mediated balancing selection. Here, we examined diversity and differentiation of neutral microsatellite loci and functional MHC class I genes in house sparrows (Passer domesticus), living in six insular and six mainland populations, and we aimed to determine whether their diversity or differentiation correlates with the diversity and the prevalence of infection of hemosporidian parasites. We found that island bird populations tended to have lower neutral genetic variability, whereas MHC variability gene was similar between island and mainland populations. Similarly, island populations tended to show greater genetic differentiation than mainland populations, especially at microsatellite markers. The maintenance of MHC genetic diversity and its less marked structure in the island populations could be attributed to balancing-selection. The greater MHC differentiation among populations was negatively correlated with similarity in blood parasites (prevalence and diversity of parasite strains) between populations. Even at low prevalence and small geographical scale, haemosporidian parasites might contribute to structure the variability of immune genes among populations of hosts.

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Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations

Cited by 35 publications

References 80 publications

Balancing selection and genetic drift create unusual patterns of MHCIIβ variation in Galápagos mockingbirds

Balancing selection and genetic drift create unusual patterns of MHCIIβ variation in Galápagos mockingbirds

Genome‐wide association and genome partitioning reveal novel genomic regions underlying variation in gastrointestinal nematode burden in a wild bird

Genetic structure in insular and mainland populations of house sparrows (Passer domesticus) and their hemosporidian parasites

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