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Selection, drift, and introgression shape MHC polymorphism in lizards.

ABSTRACT: The major histocompatibility complex (MHC) has long served as a model for the evolution of adaptive genetic diversity in wild populations. Pathogen-mediated selection is thought to be a main driver of MHC diversity, but it remains elusive to what degree selection shapes MHC diversity in complex biogeographical scenarios where other evolutionary processes (e.g. genetic drift and introgression) may also be acting. Here we focus on two closely related green lizard species, Lacerta trilineata and L. viridis, to address the evolutionary forces acting on MHC diversity in populations with different biogeographic structure. We characterized MHC class I exon 2 and exon 3, and neutral diversity (microsatellites), to study the relative importance of selection, drift, and introgression in shaping MHC diversity. As expected, positive selection was a significant force shaping the high diversity of MHC genes in both species. Moreover, introgression significantly increased MHC diversity in mainland populations, with a primary direction of gene flow from L. viridis to L. trilineata. Finally, we found significantly fewer MHC alleles in island populations, but maintained MHC sequence and functional diversity, suggesting that positive selection counteracted the effect of drift. Overall, our data support that different evolutionary processes govern MHC diversity in different biogeographical scenarios: positive selection occurs broadly while introgression acts in sympatry and drift when the population sizes decrease.

SUBMITTER: Sagonas K

PROVIDER: S-EPMC6460769 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Selection, drift, and introgression shape MHC polymorphism in lizards.

Sagonas K K Runemark A A Antoniou A A Lymberakis P P Pafilis P P Valakos E D ED Poulakakis N N Hansson B B

Heredity 20180926 4

The major histocompatibility complex (MHC) has long served as a model for the evolution of adaptive genetic diversity in wild populations. Pathogen-mediated selection is thought to be a main driver of MHC diversity, but it remains elusive to what degree selection shapes MHC diversity in complex biogeographical scenarios where other evolutionary processes (e.g. genetic drift and introgression) may also be acting. Here we focus on two closely related green lizard species, Lacerta trilineata and L. ...[more]

PMID: 30258107

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Project description:The extraordinary polymorphism of major histocompatibility complex (MHC) genes is considered a paradigm of pathogen-mediated balancing selection, although empirical evidence is still scarce. Furthermore, the relative contribution of balancing selection to shape MHC population structure and diversity, compared to that of neutral forces, as well as its interaction with other evolutionary processes such as hybridization, remains largely unclear. To investigate these issues, we analyzed adaptive (MHC-DAB gene) and neutral (11 microsatellite loci) variation in 156 brown trout (Salmo trutta complex) from six wild populations in central Italy exposed to introgression from domestic hatchery lineages (assessed with the LDH gene). MHC diversity and structuring correlated with those at microsatellites, indicating the substantial role of neutral forces. However, individuals carrying locally rare MHC alleles/supertypes were in better body condition (a proxy of individual fitness/parasite load) regardless of the zygosity status and degree of sequence dissimilarity of MHC, hence supporting balancing selection under rare allele advantage, but not heterozygote advantage or divergent allele advantage. The association between specific MHC supertypes and body condition confirmed in part this finding. Across populations, MHC allelic richness increased with increasing admixture between native and domestic lineages, indicating introgression as a source of MHC variation. Furthermore, introgression across populations appeared more pronounced for MHC than microsatellites, possibly because initially rare MHC variants are expected to introgress more readily under rare allele advantage. Providing evidence for the complex interplay among neutral evolutionary forces, balancing selection, and human-mediated introgression in shaping the pattern of MHC (functional) variation, our findings contribute to a deeper understanding of the evolution of MHC genes in wild populations exposed to anthropogenic disturbance.

Dataset Information

Selection, drift, and introgression shape MHC polymorphism in lizards.

Publications

Selection, drift, and introgression shape MHC polymorphism in lizards.

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