Postglacial Echoes: Parasite Genomics Uncover Environmental Changes in Postglacial European Lakes
Language English Country Great Britain, England Media print-electronic
Document type Journal Article
Grant support
PID2019-104908GB-I00
Government of Spain MCIN/AEI/10.13039/501100011033
169211
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
EU/PRTR PRE2020-095070
Government of Spain (MCIN/AEI/10.13039/501100011033) and European Union Next Generation
PCI2023-145950-2
Agencia Estatal de Investigación
PubMed
40667630
PubMed Central
PMC12376957
DOI
10.1111/mec.70039
Knihovny.cz E-resources
- Keywords
- Trematoda, ddRAD‐seq, demographic inference, freshwater, population genetics,
- MeSH
- Biological Evolution MeSH
- Genetic Variation MeSH
- Genomics MeSH
- Lakes parasitology MeSH
- Genetics, Population * MeSH
- Salmonidae parasitology MeSH
- Trematoda * genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Europe MeSH
Postglacial environmental changes have influenced biodiversity and species evolution, yet the genomic and demographic responses of parasites remain underexplored. This study investigates the population genetics and demographic history of the flatworm Phyllodistomum umblae, a generalist trematode at the definitive host level infecting Coregonus spp. across perialpine and subarctic postglacial lakes. Additionally, we compare its demographic patterns to Proteocephalus fallax, a whitefish specialist tapeworm, to elucidate how ecological strategies shape evolutionary responses to environmental fluctuations. Genomic data from ddRAD sequencing revealed clear genetic differentiation in P. umblae between subarctic and perialpine regions, likely driven by geographic isolation during glacial cycles. Low genetic differentiation suggests hydrological connectivity and the parasite's ability to utilise several host species as definitive hosts. Demographic inference uncovered distinct evolutionary trajectories between P. umblae and Pr. fallax. During the Last Glacial Period (~115-11 kya), P. umblae populations underwent declines, followed by rapid postglacial expansions after the Last Glacial Maximum (~15-10 kya). In contrast, Pr. fallax exhibited older historical fluctuations, including pronounced bottlenecks during the Middle Pleistocene (~300 kya). Its populations remained stable during the LGP, likely due to host persistence in glacial refugia unavailable in earlier glaciation periods. These findings align with the taxon pulse concept within the Stockholm Paradigm, highlighting how glacial cycles triggered episodic population contractions and expansions. By integrating genomic and historical data, this study (1) underscores parasites as models for understanding ecological and evolutionary processes and (2) provides insights into biodiversity resilience and adaptation to past and future environmental changes.
Cavanilles Institute of Biodiversity and Evolutionary Biology University of Valencia Valencia Spain
Department of Arctic Biology The Arctic University of Norway Tromsø Norway
Department of Invertebrates Natural History Museum of Geneva Geneva Switzerland
See more in PubMed
Adams, C. E. , Bean C. W., Dodd J. A., et al. 2016. “Inter and Intra‐Population Phenotypic and Genotypic Structuring in the European Whitefish PubMed
Agosta, S. , and Brooks D. R.. 2020. “The Stockholm Paradigm.” In The Major Metaphors of Evolution: Darwinism Then and Now, 219–242. Springer International Publishing.
Andrews, S. 2010. “FastQC A Quality Control Tool for High Throughput Sequence Data.”
Araujo, S. B. L. , Braga M. P., Brooks D. R., et al. 2015. “Understanding Host‐Switching by Ecological Fitting.” PLoS One 10: e0139225. PubMed PMC
Arcones, A. , Ponti R., Ferrer X., and Vieites D. R.. 2021. “Pleistocene Glacial Cycles as Drivers of Allopatric Differentiation in Arctic Shorebirds.” Journal of Biogeography 48: 747–759.
Bernatchez, L. , Renaut S., Whiteley A. R., et al. 2010. “On the Origin of Species: Insights From the Ecological Genomics of Lake Whitefish.” Philosophical Transactions of the Royal Society, B: Biological Sciences 365: 1783–1800. PubMed PMC
Blakeslee, A. M. H. , Haram L. E., Altman I., Kennedy K., Ruiz G. M., and Miller A. W.. 2020. “Founder Effects and Species Introductions: A Host Versus Parasite Perspective.” Evolutionary Applications 13: 559–574. PubMed PMC
Blasco‐Costa, I. , Cutmore S. C., Miller T. L., and Nolan M. J.. 2016. “Molecular Approaches to Trematode Systematics: ‘Best Practice’ and Implications for Future Study.” Systematic Parasitology 93: 295–306. PubMed
Brabec, J. , Gauthier J., Selz O. M., et al. 2024. “Testing the Radiation Cascade in Postglacial Radiations of Whitefish and Their Parasites: Founder Events and Host Ecology Drive Parasite Evolution.” Evolution Letters 8: 706–718. PubMed PMC
Brabec, J. , Rochat E. C., Knudsen R., Scholz T., and Blasco‐Costa I.. 2023. “Mining Various Genomic Resources to Resolve Old Alpha‐Taxonomy Questions: A Test of the Species Hypothesis of the PubMed
Brian, J. I. 2023. “Parasites in Biodiversity Conservation: Friend or Foe?” Trends in Parasitology 39: 618–621. PubMed
Brooks, A. J. , Bradley S. L., Edwards R. J., and Goodwyn N.. 2011. “The Palaeogeography of Northwest Europe During the Last 20,000 Years.” Journal of Maps 7: 573–587.
Butorina, T. E. , Shed'ko M. B., and Gorovaya O. Y.. 2008. “Specific Features of Ecology of Chars of the Genus
Cabanne, G. S. , Calderón L., Trujillo Arias N., et al. 2016. “Effects of Pleistocene Climate Changes on Species Ranges and Evolutionary Processes in the Neotropical Atlantic Forest.” Biological Journal of the Linnean Society 119: 856–872.
Cahill, J. A. , Green R. E., Fulton T. L., et al. 2013. “Genomic Evidence for Island Population Conversion Resolves Conflicting Theories of Polar Bear Evolution.” PLoS Genetics 9: e1003345. PubMed PMC
Castresana, J. 2000. “Selection of Conserved Blocks From Multiple Alignments for Their Use in Phylogenetic Analysis.” Molecular Biology and Evolution 17: 540–552. PubMed
Crotti, M. , Bean C. W., Gowans A. R., et al. 2021. “Complex and Divergent Histories Gave Rise to Genome‐Wide Divergence Patterns Amongst European Whitefish ( PubMed PMC
Crotti, M. , Yohannes E., Winfield I. J., Lyle A. A., Adams C. E., and Elmer K. R.. 2021. “Rapid Adaptation Through Genomic and Epigenomic Responses Following Translocations in an Endangered Salmonid.” Evolutionary Applications 14: 2470–2489. PubMed PMC
Eaton, D. A. R. , and Overcast I.. 2020. “Ipyrad: Interactive Assembly and Analysis of RADseq Datasets.” Bioinformatics 36: 2592–2594. PubMed
Ehlers, J. 2022. “North Sea and Baltic Sea in the Ice Age.” In The Ice Age, edited by Ehlers J., 307–326. Springer.
Ehlers, J. , Astakhov V., Gibbard P., Hughes P., Mangerud J., and Svendsen J.. 2023. Middle Pleistocene Glaciations in Eurasia. Elsevier.
Elliott, J. A. , and Bell V. A.. 2011. “Predicting the Potential Long‐Term Influence of Climate Change on Vendace (
Erwin, T. L. 1985. The Taxon Pulse: A General Pattern of Lineage Radiation and Extinction Among Carabid Beetles. Dr. W. Junk b.v. Publishers.
Faltýnková, A. , Pantoja C., Skírnisson K., and Kudlai O.. 2020. “Unexpected Diversity in Northern Europe: Trematodes From Salmonid Fishes in Iceland With Two New Species of Crepidostomum Braun, 1900.” Parasitology Research 119: 2439–2462. PubMed
Fox, E. A. , Wright A. E., Fumagalli M., and Vieira F. G.. 2019. “ngsLD: Evaluating Linkage Disequilibrium Using Genotype Likelihoods.” Bioinformatics 35: 3855–3856. PubMed
Gagne, R. B. , Crooks K. R., Craft M. E., et al. 2022. “Parasites as Conservation Tools.” Conservation Biology 36: e13719. PubMed
Garcia‐Erill, G. , and Albrechtsen A.. 2020. “Evaluation of Model Fit of Inferred Admixture Proportions.” Molecular Ecology Resources 20: 936–949. PubMed
Geraerts, M. , Huyse T., Barson M., et al. 2022. “Mosaic or Melting Pot: The Use of Monogeneans as a Biological Tag and Magnifying Glass to Discriminate Introduced Populations of Nile Tilapia in Sub‐Saharan Africa.” Genomics 114: 110328. PubMed
Güven, A. , and Öztürk T.. 2022. “Morphological Features of Three Species of Phyllodistomum (Trematoda: Gorgoderidae) From Some Marine Fishes in the Southern Black Sea.” Marine Biological Journal 7: 46–54.
Habel, J. C. , Drees C., Schmitt T., and Assmann T.. 2010. “Review Refugial Areas and Postglacial Colonizations in the Western Palearctic.” In Relict Species, 189–197. Springer.
Häkli, K. , Østbye K., Kahilainen K. K., Amundsen P.‐A., and Præbel K.. 2018. “Diversifying Selection Drives Parallel Evolution of Gill Raker Number and Body Size Along the Speciation Continuum of European Whitefish.” Ecology and Evolution 8: 2617–2631. PubMed PMC
Held, F. , Cheng H., Edwards R. L., Tüysüz O., Koç K., and Fleitmann D.. 2024. “Dansgaard‐Oeschger Cycles of the Penultimate and Last Glacial Period Recorded in Stalagmites From Türkiye.” Nature Communications 15: 1183. PubMed PMC
Hewitt, G. 2000. “The Genetic Legacy of the Quaternary Ice Ages.” Nature 405: 907–913. PubMed
Hewitt, G. 2004. “Genetic Consequences of Climatic Oscillations in the Quaternary.” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359: 183–195. PubMed PMC
Hoberg, E. P. , and Brooks D. R.. 2008. “A Macroevolutionary Mosaic: Episodic Host‐Switching, Geographical Colonization and Diversification in Complex Host–Parasite Systems.” Journal of Biogeography 35: 1533–1550.
Hoberg, E. P. , and Brooks D. R.. 2015. “Evolution in Action: Climate Change, Biodiversity Dynamics and Emerging Infectious Disease.” Philosophical Transactions of the Royal Society, B: Biological Sciences 370: 20130553. PubMed PMC
Hoberg, E. P. , Cook J. A., Agosta S. J., et al. 2017. “Arctic Systems in the Quaternary: Ecological Collision, Faunal Mosaics and the Consequences of a Wobbling Climate.” Journal of Helminthology 91: 409–421. PubMed
Hudson, A. , Von lanthen P., and Seehausen O.. 2011. “Rapid Parallel Adaptive Radiations From a Single Hybridogenic Ancestral Population.” Proceedings of the Royal Society B: Biological Sciences 278: 58–66. PubMed PMC
Hudson, A. , Vonlanthen P., Müller R., and Seehausen O.. 2007. “Review: The Geography of Speciation and Adaptive Radiation in Coregonines.” Advances in Limnology 60: 111–146.
Husemann, M. , Schmitt T., Zachos F. E., Ulrich W., and Habel J. C.. 2014. “Palaearctic Biogeography Revisited: Evidence for the Existence of a North African Refugium for Western Palaearctic Biota.” Journal of Biogeography 41: 81–94.
Huyse, T. , Poulin R., and Théron A.. 2005. “Speciation in Parasites: A Population Genetics Approach.” Trends in Parasitology 21: 469–475. PubMed
Johannesson, K. , Butlin R. K., Panova M., and Westram A. M.. 2020. “Mechanisms of Adaptive Divergence and Speciation in
Kafle, P. , Peller P., Massolo A., et al. 2020. “Range Expansion of Muskox Lungworms Track Rapid Arctic Warming: Implications for Geographic Colonization Under Climate Forcing.” Scientific Reports 10: 17323. PubMed PMC
Katoh, K. , Misawa K., Kuma K., and Miyata T.. 2002. “MAFFT: A Novel Method for Rapid Multiple Sequence Alignment Based on Fast Fourier Transform.” Nucleic Acids Research 30: 3059–3066. PubMed PMC
Kmentová, N. , Van Steenberge M., Thys van den Audenaerde D. F. E., et al. 2019. “Co‐Introduction Success of Monogeneans Infecting the Fisheries Target
Kolmogorov, M. , Yuan J., Lin Y., and Pevzner P. A.. 2019. “Assembly of Long, Error‐Prone Reads Using Repeat Graphs.” Nature Biotechnology 37: 540–546. PubMed
Korneliussen, T. S. , Albrechtsen A., and Nielsen R.. 2014. “ANGSD: Analysis of Next Generation Sequencing Data.” BMC Bioinformatics 15: 356. PubMed PMC
Lapierre, M. , Lambert A., and Achaz G.. 2017. “Accuracy of Demographic Inferences From the Site Frequency Spectrum: The Case of the Yoruba Population.” Genetics 206: 439–449. PubMed PMC
Lauer, T. , and Weiss M.. 2018. “Timing of the Saalian‐ and Elsterian Glacial Cycles and the Implications for Middle—Pleistocene Hominin Presence in Central Europe.” Scientific Reports 8: 5111. PubMed PMC
Li, H. , Handsaker B., Wysoker A., et al. 2009. “The Sequence Alignment/Map Format and SAMtools.” Bioinformatics 25: 2078–2079. PubMed PMC
Liu, X. , and Fu Y.‐X.. 2020. “Stairway Plot 2: Demographic History Inference With Folded SNP Frequency Spectra.” Genome Biology 21: 280. PubMed PMC
Lynch, M. 2010. “Evolution of the Mutation Rate.” Trends in Genetics 26: 345–352. PubMed PMC
Makkaveyev, A. N. , Faustova M. A., and Karpukhina N. V.. 2022. “Age and Position of the Maximum Boundary of the Scandinavian Ice Sheet in the Valdai (Weichselian, Vistulian) Glaciation and Relief in the Peripheral Area of the Ice Sheet.” Doklady Earth Sciences 507: S19–S22.
Manni, M. , Berkeley M. R., Seppey M., and Zdobnov E. M.. 2021. “BUSCO: Assessing Genomic Data Quality and Beyond.” Current Protocols 1: e323. PubMed
Meisner, J. , and Albrechtsen A.. 2018. “Inferring Population Structure and Admixture Proportions in Low‐Depth NGS Data.” Genetics 210: 719–731. PubMed PMC
Moravec, F. 2004. Metazoan Parasites of Salmonid Fishes of Europe. Academia.
Nazarizadeh, M. , Nováková M., Loot G., et al. 2023. “Historical Dispersal and Host‐Switching Formed the Evolutionary History of a Globally Distributed Multi‐Host Parasite—The PubMed
Nevado, B. , Contreras‐Ortiz N., Hughes C., and Filatov D. A.. 2018. “Pleistocene Glacial Cycles Drive Isolation, Gene Flow and Speciation in the High‐Elevation Andes.” New Phytologist 219: 779–793. PubMed
Nowak, R. M. , Jastrzębski J. P., Kuśmirek W., et al. 2019. “Hybrid De Novo Whole‐Genome Assembly and Annotation of the Model Tapeworm Hymenolepis Diminuta.” Scientific Data 6: 302. PubMed PMC
Østbye, K. , Bernatchez L., Næsje T. F., Himberg K.‐J. M., and Hindar K.. 2005. “Evolutionary History of the European Whitefish PubMed
Paradis, E. 2010. “Pegas: An R Package for Population Genetics With an Integrated–Modular Approach.” Bioinformatics 26: 419–420. PubMed
Petkevičiūtė, R. , Kudlai O., Stunžėnas V., and Stanevičiūtė G.. 2015. “Molecular and Karyological Identification and Morphological Description of Cystocercous Cercariae of Phyllodistomum Umblae and PubMed
Petkevičiūtė, R. , Stunžėnas V., and Stanevičiūtė G.. 2014. “Differentiation of European Freshwater Bucephalids (Digenea: Bucephalidae) Based on Karyotypes and DNA Sequences.” Systematic Parasitology 87: 199–212. PubMed
Præbel, K. , Knudsen R., Siwertsson A., et al. 2013. “Ecological Speciation in Postglacial European Whitefish: Rapid Adaptive Radiations Into the Littoral, Pelagic, and Profundal Lake Habitats.” Ecology and Evolution 3: 4970–4986. PubMed PMC
R Core Team . 2024. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R‐project.org/.
Reid, B. N. , and Pinsky M. L.. 2022. “Simulation‐Based Evaluation of Methods, Data Types, and Temporal Sampling Schemes for Detecting Recent Population Declines.” Integrative and Comparative Biology 62: 1849–1863. PubMed PMC
Rochat, E. C. , Brodersen J., and Blasco‐Costa I.. 2021. “Conspecific Migration and Environmental Setting Determine Parasite Infracommunities of Non‐Migratory Individual Fish.” Parasitology 148: 1057–1066. PubMed PMC
Salvi, D. , Harris D. J., Kaliontzopoulou A., Carretero M. A., and Pinho C.. 2013. “Persistence Across Pleistocene Ice Ages in Mediterranean and Extra‐Mediterranean Refugia: Phylogeographic Insights From the Common Wall Lizard.” BMC Evolutionary Biology 13: 147. PubMed PMC
Santoro, M. , Palomba M., Mattiucci S., Osca D., and Crocetta F.. 2020. “New Parasite Records for the Sunfish PubMed PMC
Schluter, D. 1996. “Adaptive Radiation Along Genetic Lines of Least Resistance.” Evolution 50: 1766–1774. PubMed
Schluter, D. 2000. The Ecology of Adaptive Radiation. OUP Oxford.
Schmitt, T. 2007. “Molecular Biogeography of Europe: Pleistocene Cycles and Postglacial Trends.” Frontiers in Zoology 4: 11. PubMed PMC
Scholz, T. 1999. “Life Cycles of Species of Proteocephalus, Parasites of Fishes in the Palearctic Region: A Review.” Journal of Helminthology 73: 1–19. PubMed
Scholz, T. , de Chambrier A., Brabec J., Knudsen R., and Blasco‐Costa I.. 2024. “Redescription of Proteocephalus Fallax La Rue, 1911 (Cestoda) and a List of Proteocephalid Tapeworms of Whitefish ( PubMed
Seehausen, O. , Butlin R. K., Keller I., et al. 2014. “Genomics and the Origin of Species.” Nature Reviews. Genetics 15: 176–192. PubMed
Selz, O. M. , Dönz C. J., Vonlanthen P., and Seehausen O.. 2020. “A Taxonomic Revision of the Whitefish of Lakes Brienz and Thun, Switzerland, With Descriptions of Four New Species (Teleostei, Coregonidae).” Zookeys 989: 79–162. PubMed PMC
Siwertsson, A. , Refsnes B., Frainer A., Amundsen P.‐A., and Knudsen R.. 2016. “Divergence and Parallelism of Parasite Infections in Arctic Charr Morphs From Deep and Shallow Lake Habitats.” Hydrobiologia 783: 131–143.
Skotte, L. , Korneliussen T. S., and Albrechtsen A.. 2013. “Estimating Individual Admixture Proportions From Next Generation Sequencing Data.” Genetics 195: 693–702. PubMed PMC
Smith, M. L. , Wallace J., Tank D. C., Sullivan J., and Carstens B. C.. 2022. “The Role of Multiple Pleistocene Refugia in Promoting Diversification in the Pacific Northwest.” Molecular Ecology 31: 4402–4416. PubMed
Soldánová, M. , Georgieva S., Roháčová J., et al. 2017. “Molecular Analyses Reveal High Species Diversity of Trematodes in a Sub‐Arctic Lake.” International Journal for Parasitology 47: 327–345. PubMed
Sromek, L. , Ylinen E., Kunnasranta M., et al. 2023. “Loss of Species and Genetic Diversity During Colonization: Insights From Acanthocephalan Parasites in Northern European Seals.” Ecology and Evolution 13: e10608. PubMed PMC
Terhorst, J. , and Song Y. S.. 2015. “Fundamental Limits on the Accuracy of Demographic Inference Based on the Sample Frequency Spectrum.” National Academy of Sciences of the United States of America 112: 7677–7682. PubMed PMC
Thorn, C. S. , Maness R. W., Hulke J. M., Delmore K. E., and Criscione C. D.. 2023. “Population Genomics of Helminth Parasites.” Journal of Helminthology 97: e29. PubMed
Vasimuddin, M. D. , Misra S., Li H., and Aluru S.. 2019. “Efficient Architecture‐Aware Acceleration of BWA‐MEM for Multicore Systems.” In 2019 IEEE International Parallel and Distributed Processing Symposium (IPDPS), 314–324. IEEE.
Vonlanthen, P. , Bittner D., Hudson A. G., et al. 2012. “Eutrophication Causes Speciation Reversal in Whitefish Adaptive Radiations.” Nature 482: 357–362. PubMed
Vurture, G. W. , Sedlazeck F. J., Nattestad M., et al. 2017. “GenomeScope: Fast Reference‐Free Genome Profiling From Short Reads.” Bioinformatics 33: 2202–2204. PubMed PMC
Wang, S. , Wang S., Luo Y., et al. 2016. “Comparative Genomics Reveals Adaptive Evolution of Asian Tapeworm in Switching to a New Intermediate Host.” Nature Communications 7: 12845. PubMed PMC
Warren, R. L. , Coombe L., Mohamadi H., et al. 2019. “ntEdit: Scalable Genome Sequence Polishing.” Bioinformatics 35: 4430–4432. PubMed PMC
Whiteman, N. K. , and Parker P. G.. 2005. “Using Parasites to Infer Host Population History: A New Rationale for Parasite Conservation.” Animal Conservation 8: 175–181.
Willis, K. J. , and Whittaker R. J.. 2000. “The Refugial Debate.” Science 287: 1406–1407. PubMed
Yanites, B. J. , Ehlers T. A., Becker J. K., Schnellmann M., and Heuberger S.. 2013. “High Magnitude and Rapid Incision From River Capture: Rhine River, Switzerland.” Journal of Geophysical Research: Earth Surface 118: 1060–1084.
Zhang, R. , Jia G., and Diao X.. 2023. “geneHapR: An R Package for Gene Haplotypic Statistics and Visualization.” BMC Bioinformatics 24: 199. PubMed PMC
Zhao, L. , Nielsen R., and Korneliussen T. S.. 2022. “distAngsd: Fast and Accurate Inference of Genetic Distances for Next‐Generation Sequencing Data.” Molecular Biology and Evolution 39: msac119. PubMed PMC