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 favor 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 nonsynonymous 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.
Reference BS11 gene sequences
Fasta sequences of 11 candidate genes under balancing selection selected from Lissotriton transcriptome (NewtBase)
balancing11.fasta
Reference control (CR) gene sequences
Fasta sequences of control genes randomly selected from Lissotriton transcriptome (NewtBase)
random178.fasta
SNP variants in BS11 genes
SNP variants called with GATK in six Lissotriton lineages and 2 outgroup species
BS11_SNPs_gatk.vcf.gz
SNP variants in CR genes
SNP variants called with GATK in six Lissotriton lineages and 2 outgroup species
CR_SNPs_gatk.vcf.gz
Genotypes for BS11 genes in Lissotriton vulgaris ampelensis
Genotypes called with GATK in Lissotriton vulgaris ampelensis
BS11_GENO_gatk_ampelensis.vcf
Genotypes for BS11 genes in Lissotriton graecus
Genotypes called with GATK in Lissotriton graecus
BS11_GENO_gatk_graecus.vcf
Genotypes for BS11 genes in Lissotriton helveticus
Genotypes called with GATK in Lissotriton helveticus
BS11_GENO_gatk_helveticus.vcf
Genotypes for BS11 genes in Lissotriton italicus
Genotypes called with GATK in Lissotriton italicus
BS11_GENO_gatk_italicus.vcf
Genotypes for BS11 genes in Lissotriton kosswigi
Genotypes called with GATK in Lissotriton kosswigi
BS11_GENO_gatk_kosswigi.vcf
Genotypes for BS11 genes in Lissotriton montandoni
Genotypes called with GATK in Lissotriton montandoni
BS11_GENO_gatk_montandoni.vcf
Genotypes for BS11 genes in Lissotriton schmidtleri
Genotypes called with GATK in Lissotriton schmidtleri
BS11_GENO_gatk_schmidtleri.vcf
Genotypes for BS11 genes in Lissotriton vulgaris vulgaris
Genotypes called with GATK in Lissotriton vulgaris vulgaris
BS11_GENO_gatk_vulgaris.vcf
Genotypes for CR genes in Lissotriton vulgaris ampelensis
Genotypes for CR genes called with GATK in Lissotriton vulgaris ampelensis
CR_GENO_gatk_ampelensis.vcf
Genotypes for CR genes in Lissotriton graecus
Genotypes for CR genes called with GATK in Lissotriton graecus
CR_GENO_gatk_graecus.vcf
Genotypes for CR genes in Lissotriton helveticus
Genotypes for CR genes called with GATK in Lissotriton helveticus
CR_GENO_gatk_helveticus.vcf
Genotypes for CR genes in Lissotriton italicus
Genotypes for CR genes called with GATK in Lissotriton italicus
CR_GENO_gatk_italicus.vcf
Genotypes for CR genes in Lissotriton kosswigi
Genotypes for CR genes called with GATK in Lissotriton kosswigi
CR_GENO_gatk_kosswigi.vcf
Genotypes for CR genes in Lissotriton montandoni
Genotypes for CR genes called with GATK in Lissotriton montandoni
CR_GENO_gatk_montandoni.vcf
Genotypes for CR genes in Lissotriton schmidtleri
Genotypes for CR genes called with GATK in Lissotriton schmidtleri
CR_GENO_gatk_schmidtleri.vcf
Genotypes for CR genes in Lissotriton vulgaris vulgaris
Genotypes for CR genes called with GATK in Lissotriton vulgaris vulgaris
CR_GENO_gatk_vulgaris.vcf
Genotypes for TAP1 gene in Lissotriton
Fasta sequences containing concatenated exon sequences of TAP1 gene genotyped in six Lissotriton lineages and an outgroup
Genotypes_TAP1.fasta
MHCI alleles
MHC class I gene alleles in Lissotriton lineages
Alleles_MHC_I_Mon_North_South.fas
MHC class I gene genotypes in Lissotriton
MHC class I gene genotypes in Lissotriton lineages
MHC_I_genotypes_Mon_North_South.xlsx
Forward simulation script NEUTRALITY M0
Forward simulation script for the scenario: Neutrality, migration = 0. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NEUTRALITY_m0.txt
SLiM simulation script NEUTRALITY M1
Forward simulation script for the scenario: Neutrality, migration M1 = 5.0E-07. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NEUTRALITY_m1.txt
SLiM simulation script NEUTRALITY M2
Forward simulation script for the scenario: Neutrality, migration M2 = 1.8E-06. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NEUTRALITY_m2.txt
SLiM simulation script NEUTRALITY M3
Forward simulation script for the scenario: Neutrality, migration M3 = 2.36E-06. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NEUTRALITY_m3.txt
SLiM simulation script moderate NFD M0
Forward simulation script for the scenario: moderate negative frequency-dependent selection, migration M0 = 0. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_medium_m0.txt
SLiM simulation script moderate NFD M1
Forward simulation script for the scenario: moderate negative frequency-dependent selection, selection strength s = 0.05, migration M1 = 5.0E-07. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_medium_m1.txt
SLiM simulation script moderate NFD M3
Forward simulation script for the scenario: moderate negative frequency-dependent selection, selection strength s = 0.05, migration M3 = 2.36E-06. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_medium_m3.txt
SLiM simulation script strong NFD M0
Forward simulation script for the scenario: strong negative frequency-dependent selection, selection strength s = 0.5, migration M0 = 0. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_strong_m0.txt
SLiM simulation script strong NFD M1
Forward simulation script for the scenario: strong negative frequency-dependent selection, selection strength s = 0.5, migration M1 = 5.0E-07. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_strong_m1.txt
SLiM simulation script strong NFD M3
Forward simulation script for the scenario: strong negative frequency-dependent selection, selection strength s = 0.5, migration M3 = 2.36E-06. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_strong_m3.txt
SLiM simulation script weak NFD M0
Forward simulation script for the scenario: weak negative frequency-dependent selection, selection strength s = 0.02, migration M0 = 0. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_weak_m0.txt
SLiM simulation script weak NFD M1
Forward simulation script for the scenario: weak negative frequency-dependent selection, selection strength s = 0.02, migration M1 = 5.0E-07. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_weak_m1.txt
SLiM simulation script weak NFD M3
Forward simulation script for the scenario: weak negative frequency-dependent selection, selection strength s = 0.02, migration M3 = 2.36E-06. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_NFD_weak_m3.txt
SLiM simulation script weak SOD M0
Forward simulation script for the scenario: weak symmetrical overdominance, selection strength s = 0.02, migration M0 = 0. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_SOD_02_m0.txt
SLiM simulation script weak SOD M1
Forward simulation script for the scenario: weak symmetrical overdominance, selection strength s = 0.02, migration M1 = 5.0E-07. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_SOD_02_m1.txt
SLiM simulation script weak SOD M3
Forward simulation script for the scenario: weak symmetrical overdominance, selection strength s = 0.02, migration M3 = 2.36E-06. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_SOD_02_m3.txt
SLiM simulation script moderate SOD M0
Forward simulation script for the scenario: moderate symmetrical overdominance, selection strength s = 0.05, migration M0 = 0. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_SOD_05_m0.txt
SLiM simulation script moderate SOD M1
Forward simulation script for the scenario: moderate symmetrical overdominance, selection strength s = 0.05, migration M1 = 5.0E-07. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_SOD_05_m1.txt
SLiM simulation script moderate SOD M3
Forward simulation script for the scenario: moderate symmetrical overdominance, selection strength s = 0.05, migration M3 = 2.36E-06. Script run in SLiM v2.5. Example command to run the script: "./slim -d simnum=00000 -d u=1.17e-7 -d locus=0 example_simulation_6_pops_00000_0.txt". example_simulation_6_pops_00000_0.txt - name of the SLiM script with one simulation specification; simnum - simulation number; u - locus mutation rate; locus - locus number.
slim_simulations_SOD_05_m3.txt