Parasites are expected to hybridise in similar ways to free-living organisms, although this may be modified by their reduced genome architecture. Recombinant strains and taxa of hybrid origin can be studied in nature where hosts come into secondary contact. Here we apply genome-wide analysis to parasites from a contact previously characterised for many individuals using classical markers. The host contact is the European house mouse hybrid zone; the parasites are lung fungus Pneumocystis and gut pinworm Syphacia. The genomic (many loci) and classical (many-individual) results are broadly consistent in scale and centring of transitions across the host hybrid zone. Whole mitogenome comparisons confirm earlier suggestions that parasite divergence is low compared to their hosts, perhaps due to reduced-genome stabilising selection. In the recombining genome, we are able to show blocks of the parasite genome of alternating host origin, including one Pneumocystis strain which appears to be an F3+ cross and one recombinant Syphacia strain found over multiple localities. Functional analyses of introgressing genes show enrichment for genes likely important for parasitic lifestyle. Our work confirms that evolutionary models of hybridisation apply equally to hosts and their parasites.

Biodiversity Research Institute University of Barcelona Barcelona Spain

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Institute of Computer Science Foundation for Research and Technology Hellas Crete Greece

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

Section of Parasitology Department of Biology Healthcare and the Environment Faculty of Pharmacy and Food Sciences University of Barcelona Barcelona Spain

Wellcome Sanger Institute Tree of Life Wellcome Genome Campus Cambridge UK

Zobrazit více v PubMed

Abbott, R. , Albach D., Ansell S., et al. 2013. “Hybridization and Speciation.” Journal of Evolutionary Biology 26, no. 2: 229–246. 10.1111/j.1420-9101.2012.02599.x. PubMed DOI

Adamson, M. L. 1984. “Haplodiploidy in DOI

Adamson, M. L. 1989. “Evolutionary Biology of the Oxyurida (Nematoda): Biofacies of a Haplodiploid Taxon.” Advances in Parasitology 28: 175–228. 10.1016/S0065-308X(08)60333-4. PubMed DOI

Adavoudi, R. , and Pilot M.. 2021. “Consequences of Hybridization in Mammals: A Systematic Review.” Genes 13, no. 1: 50. 10.3390/genes13010050. PubMed DOI PMC

Aliouat‐Denis, C. M. , Chabé M., Demanche C., et al. 2008. “ PubMed DOI

Andrews, S. 2010. “FastQC: A Quality Control Tool for High Throughput Sequence Data.” Babraham Bioinformatics. https://www.bioinformatics.babraham.ac.uk/projects/fastqc.

Arnold, B. J. , Huang I. T., and Hanage W. P.. 2022. “Horizontal Gene Transfer and Adaptive Evolution in Bacteria.” Nature Reviews Microbiology 20, no. 4: 206–218. 10.1038/s41579-021-00650-4. PubMed DOI

Baird, S. J. , and de Bellocq J. G.. 2019. “Shifting Paradigms for Studying Parasitism in Hybridising Hosts: Response to Theodosopoulos, Hund, and Taylor.” Trends in Ecology & Evolution 34, no. 5: 387–389. 10.1016/j.tree.2019.01.011. PubMed DOI

Baird, S. J. , Petružela J., Jaroň I., Škrabánek P., and Martínková N.. 2023. “Genome Polarisation for Detecting Barriers to Gene Flow.” Methods in Ecology and Evolution 14, no. 2: 512–528. 10.1111/2041-210X.14010. DOI

Baird, S. J. , Ribas A., Macholán M., Albrecht T., Piálek J., and Goüy de Bellocq J.. 2012. “Where Are the Wormy Mice? A Reexamination of Hybrid Parasitism in the European House Mouse Hybrid Zone.” Evolution 66, no. 9: 2757–2772. 10.1111/j.1558-5646.2012.01633.x. PubMed DOI

Baird, S. J. E. 1995. “A Simulation Study of Multilocus Clines.” Evolution 49, no. 6: 1038–1045. 10.1111/j.1558-5646.1995.tb04431.x. PubMed DOI

Baird, S. J. E. , and Macholán M.. 2012. “What Can the DOI

Barton, N. H. 1983. “Multilocus Clines.” Evolution 37: 454–471. 10.2307/2408260. PubMed DOI

Barton, N. H. , and Charlesworth B.. 1984. “Genetic Revolutions, Founder Effects and Speciation.” Annual Review of Ecology and Systematics 15: 133–164. 10.1146/annurev.es.15.110184.001025. DOI

Barton, N. H. , and Hewitt G. M.. 1985. “Analysis of Hybrid Zones.” Annual Review of Ecology and Systematics 16: 113–148. 10.1146/annurev.es.16.110185.000553. DOI

Bazykin, A. D. 1969. “Hypothetical Mechanism of Speciation.” Evolution 23, no. 4: 685–687. 10.2307/2406862. PubMed DOI

BBTools Development Team . n.d. https://jgi.doe.gov/data‐and‐tools/software‐tools/bbtools/.

Berger, V. W. , and Zhou Y.. 2014. Kolmogorov–Smirnov Test: Overview. Wiley StatsRef: Statistics Reference Online. 10.1002/9781118445112.stat06558. DOI

Bernt, M. , Donath A., Jühling F., et al. 2013. “Mitos: Improved PubMed DOI

Bishop, L. R. , Helman D., and Kovacs J. A.. 2012. “Discordant Antibody and Cellular Responses to PubMed DOI PMC

Brůna, T. , Hoff K. J., Lomsadze A., Stanke M., and Borodovsky M.. 2021. “BRAKER2: Automatic Eukaryotic Genome Annotation With GeneMark‐EP+ and AUGUSTUS Supported by a Protein Database.” NAR Genomics and Bioinformatics 3, no. 1: lqaa108. 10.1093/nargab/lqaa108. PubMed DOI PMC

Cissé, O. H. , Ma L., and Kovacs J. A.. 2024. “Retracing the Evolution of PubMed DOI PMC

Čížková, D. , Baird S. J., Těšíková J., et al. 2018. “Host Subspecific Viral Strains in European House Mice: Murine Cytomegalovirus in the Eastern ( PubMed DOI

Cooper, A. F., Jr. , and Van Gundy S. D.. 1970. “Metabolism of Glycogen and Neutral Lipids by PubMed PMC

Cucchi, T. , Auffray J. C., and Vigne J. D.. 2012. “On the Origin of the House Mouse Synanthropy and Dispersal in the Near East and Europe: Zooarchaeological Review and Perspectives.” In Evolution of the House Mouse, edited by Macholán M., Baird S. J. E., Munclinger P., and Piálek J., 65–93. Cambridge University Press. 10.1017/CBO9781139044547.005. DOI

Cushion, M. T. 2004. “ PubMed DOI

Danecek, P. , Bonfield J. K., Liddle J., et al. 2021. “Twelve Years of SAMtools and BCFtools.” GigaScience 10, no. 2: giab008. 10.1093/gigascience/giab008. PubMed DOI PMC

Deitsch, K. W. , Lukehart S. A., and Stringer J. R.. 2009. “Common Strategies for Antigenic Variation by Bacterial, Fungal, and Protozoan Pathogens.” Nature Reviews Microbiology 7, no. 7: 493–503. 10.1038/nrmicro2145. PubMed DOI PMC

Detwiler, J. T. , and Criscione C. D.. 2010. “An Infectious Topic in Reticulate Evolution: Introgression and Hybridization in Animal Parasites.” Genes 1, no. 1: 102–123. 10.3390/genes1010102. PubMed DOI PMC

Duvaux, L. , Belkhir K., Boulesteix M., and Boursot P.. 2011. “Isolation and Gene Flow: Inferring the Speciation History of European House Mice.” Molecular Ecology 20, no. 24: 5248–5264. 10.1111/j.1365-294X.2011.05343.x. PubMed DOI

Ebdon, S. , Laetsch D. R., Vila R., Baird S. J., and Lohse K.. 2025. “Genomic Regions of Current Low Hybridisation Mark Long‐Term Barriers to Gene Flow in Scarce Swallowtail Butterflies.” PLoS Genetics 21, no. 4: e1011655. 10.1371/journal.pgen.1011655. PubMed DOI PMC

Falush, D. , Stephens M., and Pritchard J. K.. 2007. “Inference of Population Structure Using Multilocus Genotype Data: Dominant Markers and Null Alleles.” Molecular Ecology Notes 7, no. 4: 574–578. 10.1111/j.1471-8286.2007.01758.x. PubMed DOI PMC

Fitzpatrick, B. M. 2013. “Alternative Forms for Genomic Clines.” Ecology and Evolution 3, no. 7: 1951–1966. 10.1002/ece3.609. PubMed DOI PMC

Föll, R. L. , Pleyers A., Lewandovski G. J., Wermter C., Hegemann V., and Paul R. J.. 1999. “Anaerobiosis in the Nematode PubMed DOI

Gaczorek, T. , Dudek K., Fritz U., et al. 2024. “Widespread Adaptive Introgression of Major Histocompatibility Complex Genes Across Vertebrate Hybrid Zones.” Molecular Biology and Evolution 41, no. 10: msae201. 10.1093/molbev/msae201. PubMed DOI PMC

Geneious Prime . 2024. https://www.geneious.com.

Gibbons, J. G. , Branco A. T., Godinho S. A., Yu S., and Lemos B.. 2015. “Concerted Copy Number Variation Balances Ribosomal DNA Dosage in Human and Mouse Genomes.” Proceedings of the National Academy of Sciences 112, no. 8: 2485–2490. 10.1073/pnas.1416878112. PubMed DOI PMC

Goüy de Bellocq, J. , Ribas A., and Baird S. J. E.. 2012. “New Insights Into Parasitism in the House Mouse Hybrid Zone.” In Evolution of the House Mouse, edited by Macholán M., Baird S. J. E., Munclinger P., and Piálek J., 455–481. Cambridge University Press. 10.1017/CBO9781139044547.020. DOI

Goüy de Bellocq, J. , Wasimuddin Ribas A., Bryja J., Piálek J., and Baird S. J.. 2018. “Holobiont Suture Zones: Parasite Evidence Across the European House Mouse Hybrid Zone.” Molecular Ecology 27, no. 24: 5214–5227. 10.1111/mec.14938. PubMed DOI

Guiliano, D. B. , Hall N., Jones S. J. M., et al. 2002. “Conservation of Long‐Range Synteny and Microsynteny Between the Genomes of Two Distantly Related Nematodes.” Genome Biology 3: research0057.1. 10.1186/gb-2002-3-10-research0057. PubMed DOI PMC

Heo, Y. , Wu X. L., Chen D., Ma J., and Hwu W. M.. 2014. “BLESS: Bloom Filter‐Based Error Correction Solution for High‐Throughput Sequencing Reads.” Bioinformatics 30, no. 10: 1354–1362. 10.1093/bioinformatics/btu030. PubMed DOI PMC

Hewitt, G. 2000. “The Genetic Legacy of the Quaternary Ice Ages.” Nature 405: 907–913. 10.1038/35016000. PubMed DOI

Hewitt, G. M. 1988. “Hybrid Zones‐Natural Laboratories for Evolutionary Studies.” Trends in Ecology & Evolution 3, no. 7: 158–167. 10.1016/0169-5347(88)90033-X. PubMed DOI

Hugot, J. P. 1999. “Primates and Their Pinworm Parasites: The Cameron Hypothesis Revisited.” Systematic Biology 48, no. 3: 523–546. 10.1080/106351599260120. PubMed DOI

Hugot, J. P. , Gardner S. L., and Morand S.. 1996. “The Enterobiinae Subfam. Nov. (Nematoda, Oxyurida) Pinworm Parasites of Primates and Rodents.” International Journal for Parasitology 26, no. 2: 147–159. 10.1016/0020-7519(95)00108-5. PubMed DOI

Icenhour, C. R. , Arnold J., Medvedovic M., and Cushion M. T.. 2006. “Competitive Coexistence of Two PubMed DOI

Jiang, H. , Lei R., Ding S. W., and Zhu S.. 2014. “Skewer: A Fast and Accurate Adapter Trimmer for Next‐Generation Sequencing Paired‐End Reads.” BMC Bioinformatics 15: 182. 10.1186/1471-2105-15-182. PubMed DOI PMC

Jones, E. P. , Van Der Kooij J., Solheim R., and Searle J. B.. 2010. “Norwegian House Mice ( PubMed DOI

Katoh, K. , and Standley D. M.. 2013. “MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability.” Molecular Biology and Evolution 30, no. 4: 772–780. 10.1093/molbev/mst010. PubMed DOI PMC

Keely, S. P. , Linke M. J., Cushion M. T., and Stringer J. R.. 2007. “ PubMed DOI PMC

Kim, S. C. , and Rieseberg L. H.. 1999. “Genetic Architecture of Species Differences in Annual Sunflowers: Implications for Adaptive Trait Introgression.” Genetics 153, no. 2: 965–977. 10.1093/genetics/153.2.965. PubMed DOI PMC

King, K. C. , Stelkens R. B., Webster J. P., Smith D. F., and Brockhurst M. A.. 2015. “Hybridization in Parasites: Consequences for Adaptive Evolution, Pathogenesis, and Public Health in a Changing World.” PLoS Pathogens 11, no. 9: e1005098. 10.1371/journal.ppat.1005098. PubMed DOI PMC

Kofler, R. , Pandey R. V., and Schlötterer C.. 2011. “PoPoolation2: Identifying Differentiation Between Populations Using Sequencing of Pooled DNA Samples (Pool‐Seq).” Bioinformatics 27, no. 24: 3435–3436. 10.1093/bioinformatics/btr589. PubMed DOI PMC

Komuniecki, P. R. , and Vanover L.. 1987. “Biochemical Changes During the Aerobic‐Anaerobic Transition in PubMed DOI

Kumar, S. , Stecher G., Li M., Knyaz C., and Tamura K.. 2018. “MEGA X: Molecular Evolutionary Genetics Analysis Across Computing Platforms.” Molecular Biology and Evolution 35, no. 6: 1547–1549. 10.1093/molbev/msy096. PubMed DOI PMC

Kutty, G. , Maldarelli F., Achaz G., and Kovacs J. A.. 2008. “Variation in the Major Surface Glycoprotein Genes in PubMed DOI PMC

Laetsch, D. R. , and Blaxter M. L.. 2017. “BlobTools: Interrogation of Genome Assemblies.” F1000Research 6: 1287. 10.12688/f1000research.12232.1. DOI

Lanfear, R. , Frandsen P. B., Wright A. M., Senfeld T., and Calcott B.. 2017. “PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses.” Molecular Biology and Evolution 34, no. 3: 772–773. 10.1093/molbev/msw260. PubMed DOI

Langmead, B. , and Salzberg S. L.. 2012. “Fast Gapped‐Read Alignment With Bowtie 2.” Nature Methods 9, no. 4: 357–359. 10.1038/nmeth.1923. PubMed DOI PMC

Latinne, A. , Bezé F., Delhaes L., et al. 2018. “Genetic Diversity and Evolution of PubMed DOI

Latinne, A. , Chen H. W., Kuo C. C., et al. 2021. “Revisiting the PubMed DOI

Li, H. , and Durbin R.. 2009. “Fast and Accurate Short Read Alignment With Burrows‐Wheeler Transform.” Bioinformatics 25, no. 14: 1754–1760. 10.1093/bioinformatics/btp324. PubMed DOI PMC

Lohse, K. , and Ross L.. 2015. “What Haplodiploids Can Teach Us About Hybridization and Speciation.” Molecular Ecology 24, no. 10: 5075–5077. 10.1111/mec.13393. PubMed DOI PMC

Ma, L. , Chen Z., Huang D. W., et al. 2016. “Genome Analysis of Three PubMed DOI PMC

Macholán, M. , Munclinger P., Šugerková M., et al. 2007. “Genetic Analysis of Autosomal and X‐Linked Markers Across a Mouse Hybrid Zone.” Evolution 61, no. 4: 746–771. 10.1111/j.1558-5646.2007.00065.x. PubMed DOI

Mallet, J. 2005. “Hybridization as an Invasion of the Genome.” Trends in Ecology & Evolution 20, no. 5: 229–237. 10.1016/j.tree.2005.02.010. PubMed DOI

Martin, S. H. , and Jiggins C. D.. 2017. “Interpreting the Genomic Landscape of Introgression.” Current Opinion in Genetics & Development 47: 69–74. 10.1016/j.gde.2017.08.007. PubMed DOI

Mitreva, M. , Blaxter M. L., Bird D. M., and McCarter J. P.. 2005. “Comparative Genomics of Nematodes.” Trends in Genetics 21, no. 10: 573–581. 10.1016/j.tig.2005.08.003. PubMed DOI

Moulia, C. , Aussel J. P., Bonhomme F., Boursot P., Nielsen J. T., and Renaud F.. 1991. “Wormy Mice in a Hybrid Zone: A Genetic Control of Susceptibility to Parasite Infection.” Journal of Evolutionary Biology 4, no. 4: 679–687. 10.1046/j.1420-9101.1991.4040679.x. DOI

Ottenburghs, J. , Ydenberg R. C., Van Hooft P., Van Wieren S. E., and Prins H. H.. 2015. “The Avian Hybrids Project: Gathering the Scientific Literature on Avian Hybridization.” Ibis 157, no. 4: 892–894. 10.1111/ibi.12285. DOI

Pérez‐Losada, M. , Arenas M., Galán J. C., Palero F., and González‐Candelas F.. 2015. “Recombination in Viruses: Mechanisms, Methods of Study, and Evolutionary Consequences.” Infection, Genetics and Evolution 30: 296–307. 10.1016/j.meegid.2014.12.022. PubMed DOI PMC

Petružela, J. , Bryja J., Bryjová A., et al. 2019. “Evolutionary History of PubMed DOI

Picard Tools . 2018. “Broad Institute, GitHub Repository.” http://broadinstitute.github.io/picard/.

Prjibelsky, A. , Antipov D., Meleshko D., Lapidus A., and Korobeynikov A.. 2020. “Using SPAdes De Novo Assembler.” Current Protocols in Bioinformatics 70, no. 1: e102. 10.1002/cpbi.102. PubMed DOI

Rambaut, A. 2009. “FigTree. Tree Figure Drawing Tool.” http://tree.bio.ed.ac.uk/software/figtree/.

Raufaste, N. , Orth A., Belkhir K., et al. 2005. “Inferences of Selection and Migration in the Danish House Mouse Hybrid Zone.” Biological Journal of the Linnean Society 84, no. 3: 593–616. 10.1111/j.1095-8312.2005.00457.x. DOI

Remington, C. L. 1968. “Suture‐Zones of Hybrid Interaction Between Recently Joined Biotas.” In Evolutionary Biology, edited by Dobzhansky T., Hecht M. K., and Steere W. C., 321–428. Springer. 10.1007/978-1-4684-8094-8_8. DOI

Rhind, N. , Chen Z., Yassour M., et al. 2011. “Comparative Functional Genomics of the Fission Yeasts.” Science 332, no. 6032: 930–936. 10.1126/science.1203357. PubMed DOI PMC

Rohlf, F. J. , and Sokal R. R.. 1981. “Comparing Numerical Taxonomic Studies.” Systematic Biology 30, no. 4: 459–490. 10.1093/sysbio/30.4.459. DOI

Ronquist, F. , Teslenko M., Van Der Mark P., et al. 2012. “MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space.” Systematic Biology 61, no. 3: 539–542. 10.1093/sysbio/sys029. PubMed DOI PMC

Sage, R. D. , Heyneman D., Lim K. C., and Wilson A. C.. 1986. “Wormy Mice in a Hybrid Zone.” Nature 324: 60–63. 10.1038/324060a0. PubMed DOI

Sawamura, K. 2012. “Chromatin Evolution and Molecular Drive in Speciation.” International Journal of Evolutionary Biology 2012: 301894. 10.1155/2012/301894. PubMed DOI PMC

Saz, H. J. 1971. “Facultative Anaerobiosis in the Invertebrates: Pathways and Control Systems.” American Zoologist 11, no. 1: 125–133. 10.1093/icb/11.1.125. DOI

Signorell, A. , Aho K., Alfons A., et al. 2016. DescTools: Tools for Descriptive Statistics. R Package Version 0.99.18. R Foundation for Statistical Computing. 10.32614/CRAN.package.DescTools. DOI

Sommer, R. S. , and Nadachowski A.. 2006. “Glacial Refugia of Mammals in Europe: Evidence From Fossil Records.” Mammal Review 36, no. 4: 251–265. 10.1111/j.1365-2907.2006.00093.x. DOI

Steensels, J. , Gallone B., and Verstrepen K. J.. 2021. “Interspecific Hybridization as a Driver of Fungal Evolution and Adaptation.” Nature Reviews Microbiology 19: 485–500. 10.1038/s41579-021-00537-4. PubMed DOI

Steensma, D. P. , Kyle R. A., and Shampo M. A.. 2010. “Abbie Lathrop, the “Mouse Woman of Granby”: Rodent Fancier and Accidental Genetics Pioneer.” Mayo Clinic Proceedings 85, no. 11: e83. 10.4065/mcp.2010.0647. PubMed DOI PMC

Taberlet, P. , Fumagalli L., Wust‐Saucy A. G., and Cosson J. F.. 1998. “Comparative Phylogeography and Postglacial Colonization Routes in Europe.” Molecular Ecology 7, no. 4: 453–464. 10.1046/j.1365-294X.1998.00289.x. PubMed DOI

Taylor, S. A. , and Larson E. L.. 2019. “Insights From Genomes Into the Evolutionary Importance and Prevalence of Hybridization in Nature.” Nature Ecology & Evolution 3, no. 2: 170–177. 10.1038/s41559-018-0777-y. PubMed DOI

Teeter, K. C. , Payseur B. A., Harris L. W., et al. 2008. “Genome‐Wide Patterns of Gene Flow Across a House Mouse Hybrid Zone.” Genome Research 18, no. 1: 67–76. 10.1101/gr.6757907. PubMed DOI PMC

Turner, L. M. , White M. A., Tautz D., and Payseur B. A.. 2014. “Genomic Networks of Hybrid Sterility.” PLoS Genetics 10, no. 2: e1004162. 10.1371/journal.pgen.1004162. PubMed DOI PMC

Van der Auwera, G. A. , and O'Connor B. D.. 2020. “Genomics in the Cloud: Using Docker.” In GATK, and WDL in Terra, 1st ed. O'Reilly Media.

Webster, B. L. , Diaw O. T., Seye M. M., Webster J. P., and Rollinson D.. 2013. “Introgressive Hybridization of PubMed DOI PMC

Weissenbacher‐Lang, C. , Grenl A., and Blasi B.. 2023. “Meta‐Analysis and Systematic Literature Review of the Genus PubMed DOI PMC

Wolf, Y. I. , and Koonin E. V.. 2013. “Genome Reduction as the Dominant Mode of Evolution.” BioEssays 35, no. 9: 829–837. 10.1002/bies.201300037. PubMed DOI PMC

Woolf, B. 1957. “The Log Likelihood Ratio Test (The G‐Test).” Annals of Human Genetics 21, no. 4: 397–409. 10.1111/j.1469-1809.1972.tb00293.x. PubMed DOI

Yoshida, K. , Rödelsperger C., Röseler W., et al. 2023. “Chromosome Fusions Repatterned Recombination Rate and Facilitated Reproductive Isolation During PubMed DOI PMC

Zerbino, D. R. , and Birney E.. 2008. “Velvet: Algorithms for De Novo Short Read Assembly Using de Bruijn Graphs.” Genome Research 18, no. 5: 821–829. 10.1101/gr.074492.107. PubMed DOI PMC