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.

Differential introgression across newt hybrid zones: Evidence from replicated transects

“…For four categories of candidate genes, we tested a priori expectations about their introgression compared to the genome‐wide average (Fijarczyk et al, , ; Payseur, ). Specifically, we tested for: (a) increased introgression of putative targets of balancing selection (BS genes), (b) reduced introgression of genes with elevated interspecific F ST ( F ST genes), (c) reduced introgression of genes with elevated absolute interspecific sequence divergence, d xy (d xy genes), and (d) reduced and possibly asymmetric introgression of genes showing segregation distortion (highly distorted markers) in F 2 hybrids (HDM genes).…”

“…We use broad genomic and geographical sampling to address four specific objectives: (a) test for differences in recent/ongoing introgression between the two zones, (b) assess genomic clustering of genes with similar patterns of introgression, (c) test if introgression of genes highly differentiated between species or showing segregation distortion in F 2 hybrids is restricted and (d) test for increased introgression of previously identified putative targets of balancing selection (Fijarczyk, Dudek, & Babik, ; Fijarczyk et al, ). To address the first objective, we investigated genome‐wide introgression in two transects through the IN zone and three transects through the OUT zone.…”

Massive introgression of major histocompatibility complex (MHC) genes in newt hybrid zones

“…Laboratory and bioinformatics procedures used for MHC class I genotyping were described in detail in Fijarczyk et al (). MHC class I data for a small fraction of populations (eight out of 128, Table ) were reported in Fijarczyk et al (). MHC class II was amplified with primers based on those used in Nadachowska‐Brzyska et al (), modified to include additional variation in the regions of primer annealing, as identified by transcriptome resequencing and genome walking.…”

“…However, paradoxically, convincing demonstration of introgression of these genes may be the most challenging. Genes involved in fighting pathogen assault, which often evolve under various forms of selection that maintain and promote diversity (collectively termed balancing selection), are prime candidates for adaptive introgression (Fijarczyk, Dudek, Niedzicka, & Babik, ; Schierup, Vekemans, & Charlesworth, ). This is because novel alleles may confer selective advantage and selection would favour their introgression (Phillips et al, ).…”

“…Vertebrate major histocompatibility complex (MHC) genes are a textbook example of long‐term balancing selection (Spurgin & Richardson, ) driven in a large part by Red Queen dynamics (Ejsmond & Radwan, ). Adaptive MHC introgression between hybridizing species has been inferred in several systems (Abi‐Rached et al, ; Fijarczyk et al, ; Grossen, Keller, Biebach, Croll, & International Goat Genome Consortium, ; Nadachowska‐Brzyska, Zieliński, Radwan, & Babik, ; Wegner & Eizaguirre, ), with varying strength of supporting evidence. However, studying introgression of targets of balancing selection is challenging because balancing selection itself generates patterns of variation and differentiation resembling those due to introgression, which makes distinguishing between these two processes difficult (Fijarczyk & Babik, ).…”