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Balancing selection and introgression of newt immune-response genes.

ABSTRACT: The importance of interspecific introgression as a source of adaptive variation is increasingly recognized. Theory predicts that beneficial genetic variants cross species boundaries easily even when interspecific hybridization is rare and gene flow is strongly constrained throughout the genome. However, it remains unclear whether certain classes of genes are particularly prone to adaptive introgression. Genes affected by balancing selection (BS) may constitute such a class, because forms of BS that favour novel, initially rare alleles, should facilitate introgression. We tested this hypothesis in hybridizing newts by comparing 13 genes with signatures of BS, in particular an excess of common non-synonymous polymorphisms, to the genomic background (154 genes). Parapatric hybridizing taxa were less differentiated in BS candidate genes than more closely related allopatric lineages, while the opposite was observed in the control genes. Coalescent and forward simulations that explored neutral and BS scenarios under isolation and migration showed that processes other than differential gene flow are unlikely to account for this pattern. We conclude that BS, probably involving a form of novel allele advantage, promotes introgression. This mechanism may be a source of adaptively relevant variation in hybridizing species over prolonged periods.

SUBMITTER: Fijarczyk A

PROVIDER: S-EPMC6111169 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Balancing selection and introgression of newt immune-response genes.

Fijarczyk Anna A Dudek Katarzyna K Niedzicka Marta M Babik Wiesław W

Proceedings. Biological sciences 20180815 1884

The importance of interspecific introgression as a source of adaptive variation is increasingly recognized. Theory predicts that beneficial genetic variants cross species boundaries easily even when interspecific hybridization is rare and gene flow is strongly constrained throughout the genome. However, it remains unclear whether certain classes of genes are particularly prone to adaptive introgression. Genes affected by balancing selection (BS) may constitute such a class, because forms of BS t ...[more]

PMID: 30111606

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Project description:Recently diverged species typically have incomplete reproductive barriers, allowing introgression of genetic material from one species into the genomic background of the other. The role of natural selection in preventing or promoting introgression remains contentious. Because of genomic co-adaptation, some chromosomal fragments are expected to be selected against in the new background and resist introgression. In contrast, natural selection should favor introgression for alleles at genes evolving under multi-allelic balancing selection, such as the MHC in vertebrates, disease resistance, or self-incompatibility genes in plants. Here, we test the prediction that negative, frequency-dependent selection on alleles at the multi-allelic gene controlling pistil self-incompatibility specificity in two closely related species, Arabidopsis halleri and A. lyrata, caused introgression at this locus at a higher rate than the genomic background. Polymorphism at this gene is largely shared, and we have identified 18 pairs of S-alleles that are only slightly divergent between the two species. For these pairs of S-alleles, divergence at four-fold degenerate sites (K = 0.0193) is about four times lower than the genomic background (K = 0.0743). We demonstrate that this difference cannot be explained by differences in effective population size between the two types of loci. Rather, our data are most consistent with a five-fold increase of introgression rates for S-alleles as compared to the genomic background, making this study the first documented example of adaptive introgression facilitated by balancing selection. We suggest that this process plays an important role in the maintenance of high allelic diversity and divergence at the S-locus in flowering plant families. Because genes under balancing selection are expected to be among the last to stop introgressing, their comparison in closely related species provides a lower-bound estimate of the time since the species stopped forming fertile hybrids, thereby complementing the average portrait of divergence between species provided by genomic data.

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

Balancing selection and introgression of newt immune-response genes.

Publications

Balancing selection and introgression of newt immune-response genes.

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