Interspecific introgression is a potentially important source of novel variation of adaptive significance. Although multiple cases of adaptive introgression are well documented, broader generalizations about its targets and mechanisms are lacking. Multiallelic balancing selection, particularly when acting through rare allele advantage, is an evolutionary mechanism expected to favor adaptive introgression. This is because introgressed alleles are likely to confer an immediate selective advantage, facilitating their establishment in the recipient species even in the face of strong genomic barriers to introgression. Vertebrate major histocompatibility complex genes are well-established targets of long-term multiallelic balancing selection, so widespread adaptive major histocompatibility complex introgression is expected. Here, we evaluate this hypothesis using data from 29 hybrid zones formed by fish, amphibians, squamates, turtles, birds, and mammals at advanced stages of speciation. The key prediction of more extensive major histocompatibility complex introgression compared to genome-wide introgression was tested with three complementary statistical approaches. We found evidence for widespread adaptive introgression of major histocompatibility complex genes, providing a link between the process of adaptive introgression and an underlying mechanism. Our work identifies major histocompatibility complex introgression as a general mechanism by which species can acquire novel, and possibly regain previously lost, variation that may enhance defense against pathogens and increase adaptive potential.

Biodiversité Parasitologie et Ecologie des Ecosystèmes Aquatiques Faculté des Sciences de Tunis Univ de Tunis El Manar Tunis Tunisia

Biodiversity Research Centre and Department of Zoology University of British Columbia Vancouver British Columbia Canada

Canadian Rivers Institute University of New Brunswick Fredericton New Brunswick Canada

Department of Zoology National Museum of the Czech Republic Prague Czech Republic

Institut de Systématique Evolution Biodiversité Muséum National d'Histoire Naturelle CNRS Sorbonne Université EPHE Université des Antilles Paris France

Institut des Sciences de l'Evolution Université de Montpellier Montpellier France

Institute for Ecology Evolution and Diversity Goethe University Frankfurt am Main Germany

Institute of Environmental Biology Faculty of Biology Adam Mickiewicz University Poznań Poland

Institute of Environmental Sciences Faculty of Biology Jagiellonian University Kraków Poland

Institute of Vertebrate Biology of the Czech Academy of Sciences Brno Czech Republic

Institute of Zoology and Biomedical Research Faculty of Biology Jagiellonian University Kraków Poland

Laboratory of Molecular Ecology Institute of Animal Physiology and Genetics of the Czech Academy of Sciences Liběchov Czech Republic

MARBEC Univ Montpellier 34000 Montpellier France

Museum of Zoology Senckenberg Dresden Dresden Germany

School of Biological Earth and Environmental Sciences University College Cork Cork Ireland

Senckenberg Biodiversity and Climate Research Centre Frankfurt am Main Germany

Zobrazit více v PubMed

Abi-Rached  L, Jobin  MJ, Kulkarni  S, McWhinnie  A, Dalva  K, Gragert  L, Babrzadeh  F, Gharizadeh  B, Luo  M, Plummer  FA, et al.  The shaping of modern human immune systems by multiregional admixture with archaic humans. Science. 2011:334(6052):89–94. 10.1126/science.1209202. PubMed DOI PMC

Aitken  SN, Whitlock  MC. Assisted gene flow to facilitate local adaptation to climate change. Annu Rev Ecol Evol Syst. 2013:44(1):367–388. 10.1146/annurev-ecolsys-110512-135747. DOI

Alexander  DH, Novembre  J, Lange  K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009:19(9):1655–1664. 10.1101/gr.094052.109. PubMed DOI PMC

Babik  W, Pabijan  M, Arntzen  JW, Cogalniceanu  D, Durka  W, Radwan  J. Long-term survival of a urodele amphibian despite depleted major histocompatibility complex variation. Mol Ecol. 2009:18(5):769–781. 10.1111/j.1365-294X.2008.04057.x. PubMed DOI

Baird  SJ, Goüy de Bellocq  J. Shifting paradigms for studying parasitism in hybridising hosts: response to Theodosopoulos, Hund, and Taylor. Trends Ecol Evol. 2019:34(5):387–389. 10.1016/j.tree.2019.01.011. PubMed DOI

Baird  SJ, Ribas  A, Macholán  M, Albrecht  T, Piálek  J, Goüy de Bellocq  J. Where are the wormy mice? A reexamination of hybrid parasitism in the European house mouse hybrid zone. Evolution. 2012:66(9):2757–2772. 10.1111/j.1558-5646.2012.01633.x. PubMed DOI

Barton  NH. Gene flow past a cline. Heredity (Edinb).  1979:43(3):333–339. 10.1038/hdy.1979.86. DOI

Barton  NH. Multilocus clines. Evolution. 1983:37(3):454–471. 10.2307/2408260. PubMed DOI

Barton  NH. On the completion of speciation. Philos Trans R Soc Lond B. 2020:375(1806):20190530. 10.1098/rstb.2019.0530. PubMed DOI PMC

Barton  N, Bengtsson  BO. The barrier to genetic exchange between hybridising populations. Heredity (Edinb).  1986:57(3):357–376. 10.1038/hdy.1986.135. PubMed DOI

Bates  D, Maechler  M, Jagan  M. Matrix: sparse and dense matrix classes and methods. R package version 1.7. 2024. https://CRAN.R-project.org/package=Matrix.

Bell  G. Evolutionary rescue and the limits of adaptation. Philos Trans R Soc Lond B. 2013:368(1610):20120080. 10.1098/rstb.2012.0080. PubMed DOI PMC

Benzekri  H, Armesto  P, Cousin  X, Rovira  M, Crespo  D, Merlo  MA, Mazurais  D, Bautista  R, Guerrero-Fernández  D, Fernandez-Pozo  N, et al.  De novo assembly, characterization and functional annotation of Senegalese sole (Solea senegalensis) and common sole (Solea solea) transcriptomes: integration in a database and design of a microarray. BMC Genomics. 2014:15(1):952. 10.1186/1471-2164-15-952. PubMed DOI PMC

Botta-Dukát  Z. Cautionary note on calculating standardized effect size (SES) in randomization test. Commun Ecol. 2018:19(1):77–83. 10.1556/168.2018.19.1.8. DOI

Buerkle  CA. Maximum-likelihood estimation of a hybrid index based on molecular markers. Mol Ecol Notes. 2005:5(3):684–687. 10.1111/j.1471-8286.2005.01011.x. DOI

Butlin  RK, Smadja  CM. Coupling, reinforcement, and speciation. Am Nat. 2018:191(2):155–172. 10.1086/695136. PubMed DOI

Camacho  C, Coulouris  G, Avagyan  V, Ma  N, Papadopoulos  J, Bealer  K, Madden  TL. BLAST+: architecture and applications. BMC Bioinf. 2009:10(1):421–429. 10.1186/1471-2105-10-421. PubMed DOI PMC

Castric  V, Bechsgaard  J, Schierup  MH, Vekemans  X. Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genet. 2008:4(8):e1000168. 10.1371/journal.pgen.1000168. PubMed DOI PMC

Cohen  J. Statistical power analysis for the behavioral sciences. Hillsdale (NJ): Lawrence Erlbaum; 1988.

Cunningham  F, Allen  JE, Allen  J, Alvarez-Jarreta  J, Amode  MR, Armean  IM, Austine-Orimoloye  O, Azov  AG, Barnes  I, Bennett  R, et al.  Ensembl 2022. Nucl Acid Res. 2022:50(D1):D988–D995. 10.1093/nar/gkab1049. PubMed DOI PMC

De Coster  W, Weissensteiner  MH, Sedlazeck  FJ. Towards population-scale long-read sequencing. Nat Rev Genet. 2021:22(9):572–587. 10.1038/s41576-021-00367-3. PubMed DOI PMC

Dendrou  CA, Petersen  J, Rossjohn  J, Fugger  L. HLA variation and disease. Nat Rev Immun. 2018:18(5):325–339. 10.1038/nri.2017.143. PubMed DOI

Derryberry  EP, Derryberry  GE, Maley  JM, Brumfield  RT. HZAR: hybrid zone analysis using an R software package. Mol Ecol Res. 2014:14(3):652–663. 10.1111/1755-0998.12209. PubMed DOI

Dilthey  AT. State-of-the-art genome inference in the human MHC. Int J Biochem Cell Biol. 2021:131:105882. 10.1016/j.biocel.2020.105882. PubMed DOI

Dudek  K, Gaczorek  T, Zieliński  P, Babik  W. Massive introgression of MHC genes in newt hybrid zones. Mol Ecol. 2019:28(21):4798–4810. 10.1111/mec.15254. PubMed DOI

Ebert  P, Audano  PA, Zhu  Q, Rodriguez-Martin  B, Porubsky  D, Bonder  MJ, Sulovari  A, Ebler  J, Zhou  W, Serra Mari  R, et al.  Haplotype-resolved diverse human genomes and integrated analysis of structural variation. Science. 2021:372(6537):eabf7117. 10.1126/science.abf7117. PubMed DOI PMC

Edelman  NB, Mallet  J. Prevalence and adaptive impact of introgression. Annu Rev Genet. 2021:55(1):265–283. 10.1146/annurev-genet-021821-020805. PubMed DOI

Eizenga  JM, Novak  AM, Sibbesen  JA, Heumos  S, Ghaffaari  A, Hickey  G, Chang  X, Seaman  JD, Rounthwaite  R, Ebler  J, et al.  Pangenome graphs. Annu Rev Genom Hum Genet. 2020:21(1):139–162. 10.1146/annurev-genom-120219-080406. PubMed DOI PMC

Ejsmond  MJ, Phillips  KP, Babik  W, Radwan  J. The role of MHC supertypes in promoting trans-species polymorphism remains an open question. Nat Comm. 2018:9(1):4362. 10.1038/s41467-018-06821-x. PubMed DOI PMC

Enard  D, Petrov  DA. Evidence that RNA viruses drove adaptive introgression between Neanderthals and modern humans. Cell. 2018:175(2):360–371.e13. 10.1016/j.cell.2018.08.034. PubMed DOI PMC

Fijarczyk  A, Babik  W. Detecting balancing selection in genomes: limits and prospects. Mol Ecol. 2015:24(14):3529–3545. 10.1111/mec.13226. PubMed DOI

Fijarczyk  A, Dudek  K, Niedzicka  M, Babik  W. Balancing selection and introgression of newt immune-response genes. Proc Biol Sci.  2018:285(1884):20180819. 10.1098/rspb.2018.0819. PubMed DOI PMC

Fitzpatrick  BM. Alternative forms for genomic clines. Ecol Evol. 2013:3(7):1951–1966. 10.1002/ece3.609. PubMed DOI PMC

Gaczorek  TS, Chechetkin  M, Dudek  K, Caeiro-Dias  G, Crochet  PA, Geniez  P, Pinho  C, Babik  W. Widespread introgression of MHC genes in Iberian Podarcis lizards. Mol Ecol. 2023a:32(14):4003–4017. 10.1111/mec.16974. PubMed DOI

Gaczorek  TS, Marszałek  M, Dudek  K, Arntzen  JW, Wielstra  B, Babik  W. Interspecific introgression of MHC genes in Triturus newts: evidence from multiple contact zones. Mol Ecol. 2023b:32(4):867–880. 10.1111/mec.16804. PubMed DOI PMC

Giska  I, Farelo  L, Pimenta  J, Seixas  FA, Ferreira  MS, Marques  JP, Miranda  I, Letty  J, Jenny  H, Hackländer  K, et al.  Introgression drives repeated evolution of winter coat color polymorphism in hares. Proc Natl Acad Sci U S A.  2019:116(48):24150–24156. 10.1073/pnas.1910471116. PubMed DOI PMC

Gompert  Z, Buerkle  CA. Bayesian estimation of genomic clines. Mol Ecol. 2011:20(10):2111–2127. 10.1111/j.1365-294X.2011.05074.x. PubMed DOI

Gompert  Z, Mandeville  EG, Buerkle  CA. Analysis of population genomic data from hybrid zones. Annu Rev Ecol Evol Syst. 2017:48(1):207–229. 10.1146/annurev-ecolsys-110316-022652. DOI

Gotelli  NJ, McCabe  DJ. Species co-occurrence: a meta-analysis of JM Diamond's assembly rules model. Ecology. 2002:83(8):2091–2096. 10.1890/0012-9658(2002)083[2091:SCOAMA]2.0.CO;2. DOI

Gower  G, Picazo  PI, Fumagalli  M, Racimo  F. Detecting adaptive introgression in human evolution using convolutional neural networks. eLife. 2021:10:e64669. 10.7554/eLife.64669. PubMed DOI PMC

Grabherr  MG, Haas  BJ, Yassour  M, Levin  JZ, Thompson  DA, Amit  I, Adiconis  X, Fan  L, Raychowdhury  R, Zeng  Q, et al.  Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotech. 2011:29(7):644–652. 10.1038/nbt.1883. PubMed DOI PMC

Greenbaum  G, Getz  WM, Rosenberg  NA, Feldman  MW, Hovers  E, Kolodny  O. Disease transmission and introgression can explain the long-lasting contact zone of modern humans and Neanderthals. Nat Commun. 2019:10(1):5003. 10.1038/s41467-019-12862-7. PubMed DOI PMC

Grossen  C, Keller  L, Biebach  I, Croll  D, Consortium IGG . Introgression from domestic goat generated variation at the major histocompatibility complex of Alpine ibex. PLoS Genet. 2014:10(6):e1004438. 10.1371/journal.pgen.1004438. PubMed DOI PMC

Haller  BC, Messer  PW. SLiM 4: multispecies eco-evolutionary modeling. Am Nat. 2023:201(5):E127–E139. 10.1086/723601. PubMed DOI PMC

Hamilton  JA, Miller  JM. Adaptive introgression as a resource for management and genetic conservation in a changing climate. Conserv Biol. 2016:30(1):33–41. 10.1111/cobi.12574. PubMed DOI

Hedges  LV. Distribution theory for Glass's estimator of effect size and related estimators. J Educ Stat. 1981:6(2):107–128. 10.3102/10769986006002107. DOI

Hedrick  PW. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol. 2013:22(18):4606–4618. 10.1111/mec.12415. PubMed DOI

Herdegen-Radwan  M, Phillips  KP, Babik  W, Mohammed  RS, Radwan  J. Balancing selection versus allele and supertype turnover in MHC class II genes in guppies. Heredity (Edinb).  2021:126(3):548–560. 10.1038/s41437-020-00369-7. PubMed DOI PMC

Irisarri  I, Baurain  D, Brinkmann  H, Delsuc  F, Sire  J-Y, Kupfer  A, Petersen  J, Jarek  M, Meyer  A, Vences  M, et al.  Phylotranscriptomic consolidation of the jawed vertebrate timetree. Nat Ecol Evol. 2017:1(9):1370–1378. 10.1038/s41559-017-0240-5. PubMed DOI PMC

Kulmuni  J, Butlin  RK, Lucek  K, Savolainen  V, Westram  AM. Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers. Philos Trans R Soc Lond B. 2020:375(1806):20190528. 10.1098/rstb.2019.0528. PubMed DOI PMC

Kumar  S, Stecher  G, Suleski  M, Hedges  SB. TimeTree: a resource for timelines, timetrees, and divergence times. Mol Biol Evol. 2017:34(7):1812–1819. 10.1093/molbev/msx116. PubMed DOI

Li  T, Du  D, Zhang  D, Lin  Y, Ma  J, Zhou  M, Meng  W, Jin  Z, Chen  Z, Yuan  H, et al.  CRISPR-based targeted haplotype-resolved assembly of a megabase region. Nat Commun. 2023:14(1):22. 10.1038/s41467-022-35389-w. PubMed DOI PMC

Liao  W-W, Asri  M, Ebler  J, Doerr  D, Haukness  M, Hickey  G, Lu  S, Lucas  JK, Monlong  J, Abel  HJ, et al.  A draft human pangenome reference. Nature. 2023:617(7960):312–324. 10.1038/s41586-023-05896-x. PubMed DOI PMC

Maccari  G, Robinson  J, Ballingall  K, Guethlein  LA, Grimholt  U, Kaufman  J, Ho  C-S, De Groot  NG, Flicek  P, Bontrop  RE, et al.  IPD-MHC 2.0: an improved inter-species database for the study of the major histocompatibility complex. Nucl Acid Res. 2017:45(D1):D860–D864. 10.1093/nar/gkw1050. PubMed DOI PMC

Marková  S, Horníková  M, Lanier  HC, Henttonen  H, Searle  JB, Weider  LJ, Kotlík  P. High genomic diversity in the bank vole at the northern apex of a range expansion: the role of multiple colonizations and end-glacial refugia. Mol Ecol. 2020:29(9):1730–1744. 10.1111/mec.15427. PubMed DOI

Marková  S, Lanier  HC, Escalante  MA, da Cruz  MO, Horníková  M, Konczal  M, Weider  LJ, Searle  JB, Kotlík  P. Local adaptation and future climate vulnerability in a wild rodent. Nat Comm. 2023:14(1):7840. 10.1038/s41467-023-43383-z. PubMed DOI PMC

McConnell  SC, Hernandez  KM, Wcisel  DJ, Kettleborough  RN, Stemple  DL, Yoder  JA, Andrade  J, de Jong  JL. Alternative haplotypes of antigen processing genes in zebrafish diverged early in vertebrate evolution. Proc Natl Acad Sci U S A.  2016:113(34):E5014–E5023. 10.1073/pnas.1607602113. PubMed DOI PMC

Migalska  M, Przesmycka  K, Alsarraf  M, Bajer  A, Behnke-Borowczyk  J, Grzybek  M, Behnke  JM, Radwan  J. Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics. Mol Ecol. 2022:31(12):3400–3415. 10.1111/mec.16486. PubMed DOI PMC

Migalska  M, Sebastian  A, Konczal  M, Kotlík  P, Radwan  J. De novo transcriptome assembly facilitates characterisation of fast-evolving gene families, MHC class I in the bank vole (Myodes glareolus). Heredity (Edinb).  2017:118(4):348–357. 10.1038/hdy.2016.105. PubMed DOI PMC

Migalska  M, Sebastian  A, Radwan  J. Major histocompatibility complex class I diversity limits the repertoire of T cell receptors. Proc Natl Acad Sci U S A.  2019:116(11):5021–5026. 10.1073/pnas.1807864116. PubMed DOI PMC

Moran  BM, Payne  C, Langdon  Q, Powell  DL, Brandvain  Y, Schumer  M. The genomic consequences of hybridization. eLife. 2021:10:e69016. 10.7554/eLife.69016. PubMed DOI PMC

Murphy  K, Weaver  C, Berg  L. Janeway's immunobiology. New York: Norton; 2022.

Nosil  P, Feder  JL, Flaxman  SM, Gompert  Z. Tipping points in the dynamics of speciation. Nat Ecol Evol. 2017:1(2):0001. 10.1038/s41559-016-0001. PubMed DOI

Nürnberger  B, Baird  SJ, Čížková  D, Bryjová  A, Mudd  AB, Blaxter  ML, Szymura  JM. A dense linkage map for a large repetitive genome: discovery of the sex-determining region in hybridizing fire-bellied toads (Bombina bombina and Bombina variegata). G3. 2021:11:(12):jkab286. 10.1093/g3journal/jkab286. PubMed DOI PMC

Pabijan  M, Wandycz  A, Hofman  S, Węcek  K, Piwczyński  M, Szymura  JM. Complete mitochondrial genomes resolve phylogenetic relationships within Bombina (Anura: Bombinatoridae). Mol Phyl Evol. 2013:69(1):63–74. 10.1016/j.ympev.2013.05.007. PubMed DOI

Palomar  G, Dudek  K, Migalska  M, Arntzen  J, Ficetola  GF, Jelić  D, Jockusch  E, Martínez-Solano  I, Matsunami  M, Shaffer  HB, et al.  Coevolution between MHC class I and antigen-processing genes in salamanders. Mol Biol Evol. 2021:38(11):5092–5106. 10.1093/molbev/msab237. PubMed DOI PMC

Paradis  E, Schliep  K. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019:35(3):526–528. 10.1093/bioinformatics/bty633. PubMed DOI

Payseur  BA. Using differential introgression in hybrid zones to identify genomic regions involved in speciation. Mol Ecol Res. 2010:10(5):806–820. 10.1111/j.1755-0998.2010.02883.x. PubMed DOI

Phillips  KP, Cable  J, Mohammed  RS, Herdegen-Radwan  M, Raubic  J, Przesmycka  KJ, van Oosterhout  C, Radwan  J. Immunogenetic novelty confers a selective advantage in host–pathogen coevolution. Proc Natl Acad Sci U S A.  2018:115(7):1552–1557. 10.1073/pnas.1708597115. PubMed DOI PMC

Piálek  J, Barton  NH. The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics. 1997:145(2):493–504. 10.1093/genetics/145.2.493. PubMed DOI PMC

Pierini  F, Lenz  TL. Divergent allele advantage at human MHC genes: signatures of past and ongoing selection. Mol Biol Evol. 2018:35(9):2145–2158. 10.1093/molbev/msy116. PubMed DOI PMC

Pinheiro  J, Bates  D, R Core Team . 2023. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3. https://CRAN.R-project.org/package=nlme.

Pishesha  N, Harmand  TJ, Ploegh  HL. A guide to antigen processing and presentation. Nat Rev Immun. 2022:22(12):751–764. 10.1038/s41577-022-00707-2. PubMed DOI

Pritchard  JK, Stephens  M, Donnelly  P. Inference of population structure using multilocus genotype data. Genetics. 2000:155(2):945–959. 10.1093/genetics/155.2.945. PubMed DOI PMC

Rabosky  DL, Chang  J, Title  PO, Cowman  PF, Sallan  L, Friedman  M, Kaschner  K, Garilao  C, Near  TJ, Coll  M, et al.  An inverse latitudinal gradient in speciation rate for marine fishes. Nature. 2018:559(7714):392–395. 10.1038/s41586-018-0273-1. PubMed DOI

Radwan  J, Babik  W, Kaufman  J, Lenz  TL, Winternitz  J. Advances in the evolutionary understanding of MHC polymorphism. Trends Genet. 2020:36(4):298–311. 10.1016/j.tig.2020.01.008. PubMed DOI

Ralls  K, Ballou  JD, Dudash  MR, Eldridge  MD, Fenster  CB, Lacy  RC, Sunnucks  P, Frankham  R. Call for a paradigm shift in the genetic management of fragmented populations. Conserv Lett. 2018:11(2):e12412. 10.1111/conl.12412. DOI

Ravinet  M, Yoshida  K, Shigenobu  S, Toyoda  A, Fujiyama  A, Kitano  J. The genomic landscape at a late stage of stickleback speciation: high genomic divergence interspersed by small localized regions of introgression. PLoS Genet. 2018:14(5):e1007358. 10.1371/journal.pgen.1007358. PubMed DOI PMC

Rosenberg  MS, Rothstein  HR, Gurevitch  J. Effect sizes: conventional choices and calculations. In: Handbook of meta-analysis in ecology and evolution. Princeton: Princeton University Press; 2013. p. 61–71.

Rousselle  M, Simion  P, Tilak  M-K, Figuet  E, Nabholz  B, Galtier  N. Is adaptation limited by mutation? A timescale-dependent effect of genetic diversity on the adaptive substitution rate in animals. PLoS Genet. 2020:16(4):e1008668. 10.1371/journal.pgen.1008668. PubMed DOI PMC

Sato  A, Figueroa  F, Murray  BW, Málaga-Trillo  E, Zaleska-Rutczynska  Z, Sültmann  H, Toyosawa  S, Wedekind  C, Steck  N, Klein  J. Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes.  Immunogenetics. 2000:51(2):108–124. 10.1007/s002510050019. PubMed DOI

Schierup  MH, Vekemans  X, Charlesworth  D. The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet Res. 2000:76(1):51–62. 10.1017/S0016672300004535. PubMed DOI

Schöneberg  Y, Winter  S, Arribas  O, Di Nicola  MR, Master  M, Owens  JB, Rovatsos  M, Wüster  W, Janke  A, Fritz  U. Genomics reveals broad hybridization in deeply divergent Palearctic grass and water snakes (Natrix spp.). Mol Phyl Evol. 2023:184:107787. 10.1016/j.ympev.2023.107787. PubMed DOI

Sebastian  A, Herdegen  M, Migalska  M, Radwan  J. Amplisas: a web server for multilocus genotyping using next-generation amplicon sequencing data. Mol Ecol Res. 2016:16(2):498–510. 10.1111/1755-0998.12453. PubMed DOI

Seneviratne  SS, Davidson  P, Martin  K, Irwin  DE. Low levels of hybridization across two contact zones among three species of woodpeckers (Sphyrapicus sapsuckers). J Avian Biol. 2016:47(6):887–898. 10.1111/jav.00946. DOI

Setter  D, Mousset  S, Cheng  X, Nielsen  R, DeGiorgio  M, Hermisson  J. VolcanoFinder: genomic scans for adaptive introgression. PLoS Genet. 2020:16(6):e1008867. 10.1371/journal.pgen.1008867. PubMed DOI PMC

Skotte  L, Korneliussen  TS, Albrechtsen  A. Estimating individual admixture proportions from next generation sequencing data. Genetics. 2013:195(3):693–702. 10.1534/genetics.113.154138. PubMed DOI PMC

Song  Y, Endepols  S, Klemann  N, Richter  D, Matuschka  FR, Shih  CH, Nachman  MW, Kohn  MH. Adaptive introgression of anticoagulant rodent poison resistance by hybridization between old world mice. Curr Biol. 2011:21(15):1296–1301. 10.1016/j.cub.2011.06.043. PubMed DOI PMC

Spurgin  LG, Richardson  DS. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc Biol Sci.  2010:277(1684):979–988. 10.1098/rspb.2009.2084. PubMed DOI PMC

Svedberg  J, Shchur  V, Reinman  S, Nielsen  R, Corbett-Detig  R. Inferring adaptive introgression using hidden Markov models. Mol Biol Evol. 2021:38(5):2152–2165. 10.1093/molbev/msab014. PubMed DOI PMC

Szymura  JM, Barton  NH. Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and B. variegata, near Cracow in southern Poland. Evolution. 1986:40(6):1141–1159. 10.1111/j.1558-5646.1986.tb05740.x. PubMed DOI

Theodosopoulos  AN, Hund  AK, Taylor  SA. Parasites and host species barriers in animal hybrid zones. Trends Ecol Evol. 2019:34(1):19–30. 10.1016/j.tree.2018.09.011. PubMed DOI

van Dijk  EL, Naquin  D, Gorrichon  K, Jaszczyszyn  Y, Ouazahrou  R, Thermes  C, Hernandez  C. Genomics in the long-read sequencing era. Trends Genet. 2023:39(9):649–671. 10.1016/j.tig.2023.04.006. PubMed DOI

Westerdahl  H, Mellinger  S, Sigeman  H, Kutschera  VE, Proux-Wéra  E, Lundberg  M, Weissensteiner  M, Churcher  A, Bunikis  I, Hansson  B, et al.  The genomic architecture of the passerine MHC region: high repeat content and contrasting evolutionary histories of single copy and tandemly duplicated MHC genes. Mol Ecol Res. 2022:22(6):2379–2395. 10.1111/1755-0998.13614. PubMed DOI

Whitney  KD, Randell  RA, Rieseberg  LH. Adaptive introgression of herbivore resistance traits in the weedv sunflower Helianthus annuus. Am Nat. 2006:167(6):794–807. 10.1086/504606. PubMed DOI

Wielstra  B, McCartney-Melstad  E, Arntzen  J, Butlin  RK, Shaffer  HB. Phylogenomics of the adaptive radiation of Triturus newts supports gradual ecological niche expansion towards an incrementally aquatic lifestyle. Mol Phyl Evol. 2019:133:120–127. 10.1016/j.ympev.2018.12.032. PubMed DOI

Yang  W, Feiner  N, Pinho  C, While  GM, Kaliontzopoulou  A, Harris  DJ, Salvi  D, Uller  T. Extensive introgression and mosaic genomes of Mediterranean endemic lizards. Nat Commun. 2021:12(1):2762. 10.1038/s41467-021-22949-9. PubMed DOI PMC

Zieliński  P, Dudek  K, Arntzen  JW, Palomar  G, Niedzicka  M, Fijarczyk  A, Liana  M, Cogǎlniceanu  D, Babik  W. Differential introgression across newt hybrid zones—evidence from replicated transects. Mol Ecol. 2019:28(21):4811–4824. 10.1111/mec.15251. PubMed DOI