IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49726-8.html
   My bibliography  Save this article

Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean

Author

Listed:
  • Luca Cornetti

    (University of Basel
    Syngenta Crop Protection AG)

  • Peter D. Fields

    (University of Basel)

  • Louis Du Pasquier

    (University of Basel)

  • Dieter Ebert

    (University of Basel)

Abstract

Balancing selection is an evolutionary process that maintains genetic polymorphisms at selected loci and strongly reduces the likelihood of allele fixation. When allelic polymorphisms that predate speciation events are maintained independently in the resulting lineages, a pattern of trans-species polymorphisms may occur. Trans-species polymorphisms have been identified for loci related to mating systems and the MHC, but they are generally rare. Trans-species polymorphisms in disease loci are believed to be a consequence of long-term host-parasite coevolution by balancing selection, the so-called Red Queen dynamics. Here we scan the genomes of three crustaceans with a divergence of over 15 million years and identify 11 genes containing identical-by-descent trans-species polymorphisms with the same polymorphisms in all three species. Four of these genes display molecular footprints of balancing selection and have a function related to immunity. Three of them are located in or close to loci involved in resistance to a virulent bacterial pathogen, Pasteuria, with which the Daphnia host is known to coevolve. This provides rare evidence of trans-species polymorphisms for loci known to be functionally relevant in interactions with a widespread and highly specific parasite. These findings support the theory that specific antagonistic coevolution is able to maintain genetic diversity over millions of years.

Suggested Citation

  • Luca Cornetti & Peter D. Fields & Louis Du Pasquier & Dieter Ebert, 2024. "Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49726-8
    DOI: 10.1038/s41467-024-49726-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49726-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49726-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Olivier Delaneau & Jean-François Zagury & Matthew R. Robinson & Jonathan L. Marchini & Emmanouil T. Dermitzakis, 2019. "Accurate, scalable and integrative haplotype estimation," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    2. Gil McVean, 2009. "A Genealogical Interpretation of Principal Components Analysis," PLOS Genetics, Public Library of Science, vol. 5(10), pages 1-10, October.
    3. Christophe Eizaguirre & Tobias L. Lenz & Martin Kalbe & Manfred Milinski, 2012. "Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations," Nature Communications, Nature, vol. 3(1), pages 1-6, January.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Estavoyer, Maxime & François, Olivier, 2022. "Theoretical analysis of principal components in an umbrella model of intraspecific evolution," Theoretical Population Biology, Elsevier, vol. 148(C), pages 11-21.
    2. Pei-Kuan Cong & Wei-Yang Bai & Jin-Chen Li & Meng-Yuan Yang & Saber Khederzadeh & Si-Rui Gai & Nan Li & Yu-Heng Liu & Shi-Hui Yu & Wei-Wei Zhao & Jun-Quan Liu & Yi Sun & Xiao-Wei Zhu & Pian-Pian Zhao , 2022. "Genomic analyses of 10,376 individuals in the Westlake BioBank for Chinese (WBBC) pilot project," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Ralph, Peter L., 2019. "An empirical approach to demographic inference with genomic data," Theoretical Population Biology, Elsevier, vol. 127(C), pages 91-101.
    4. Peña-Malavera Andrea & Bruno Cecilia & Fernandez Elmer & Balzarini Monica, 2014. "Comparison of algorithms to infer genetic population structure from unlinked molecular markers," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 13(4), pages 391-402, August.
    5. Xiaojun Mao & Somak Dutta & Raymond K. W. Wong & Dan Nettleton, 2020. "Adjusting for Spatial Effects in Genomic Prediction," Journal of Agricultural, Biological and Environmental Statistics, Springer;The International Biometric Society;American Statistical Association, vol. 25(4), pages 699-718, December.
    6. Bryc, Katarzyna & Bryc, Wlodek & Silverstein, Jack W., 2013. "Separation of the largest eigenvalues in eigenanalysis of genotype data from discrete subpopulations," Theoretical Population Biology, Elsevier, vol. 89(C), pages 34-43.
    7. Oscar Lao & Fan Liu & Andreas Wollstein & Manfred Kayser, 2014. "GAGA: A New Algorithm for Genomic Inference of Geographic Ancestry Reveals Fine Level Population Substructure in Europeans," PLOS Computational Biology, Public Library of Science, vol. 10(2), pages 1-11, February.
    8. Lijing Tang & Benjamin Swedlund & Sébastien Dupont & Chad Harland & Gabriel Costa Monteiro Moreira & Keith Durkin & Maria Artesi & Eric Mullaart & Arnaud Sartelet & Latifa Karim & Wouter Coppieters & , 2024. "GWAS reveals determinants of mobilization rate and dynamics of an active endogenous retrovirus of cattle," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Robin J. Hofmeister & Simone Rubinacci & Diogo M. Ribeiro & Alfonso Buil & Zoltán Kutalik & Olivier Delaneau, 2022. "Parent-of-Origin inference for biobanks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Alexander Köhler & Marvin Kahra & Michael Breuß, 2024. "A First Approach to Quantum Logical Shape Classification Framework," Mathematics, MDPI, vol. 12(11), pages 1-21, May.
    11. Marie Louis & Petra Korlević & Milaja Nykänen & Frederick Archer & Simon Berrow & Andrew Brownlow & Eline D. Lorenzen & Joanne O’Brien & Klaas Post & Fernando Racimo & Emer Rogan & Patricia E. Rosel &, 2023. "Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    12. Junhui Yuan & Sanjie Jiang & Jianbo Jian & Mingyu Liu & Zhen Yue & Jiabao Xu & Juan Li & Chunyan Xu & Lihong Lin & Yi Jing & Xiaoxiao Zhang & Haixin Chen & Linjuan Zhang & Tao Fu & Shuiyan Yu & Zhangy, 2022. "Genomic basis of the giga-chromosomes and giga-genome of tree peony Paeonia ostii," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    13. Xinkai Tong & Dong Chen & Jianchao Hu & Shiyao Lin & Ziqi Ling & Huashui Ai & Zhiyan Zhang & Lusheng Huang, 2023. "Accurate haplotype construction and detection of selection signatures enabled by high quality pig genome sequences," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    14. Bárbara Sousa da Mota & Simone Rubinacci & Diana Ivette Cruz Dávalos & Carlos Eduardo G. Amorim & Martin Sikora & Niels N. Johannsen & Marzena H. Szmyt & Piotr Włodarczak & Anita Szczepanek & Marcin M, 2023. "Imputation of ancient human genomes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Parker C. Wilson & Yoshiharu Muto & Haojia Wu & Anil Karihaloo & Sushrut S. Waikar & Benjamin D. Humphreys, 2022. "Multimodal single cell sequencing implicates chromatin accessibility and genetic background in diabetic kidney disease progression," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    16. Priya Moorjani & Nick Patterson & Joel N Hirschhorn & Alon Keinan & Li Hao & Gil Atzmon & Edward Burns & Harry Ostrer & Alkes L Price & David Reich, 2011. "The History of African Gene Flow into Southern Europeans, Levantines, and Jews," PLOS Genetics, Public Library of Science, vol. 7(4), pages 1-13, April.
    17. Seppe Goovaerts & Hanne Hoskens & Ryan J. Eller & Noah Herrick & Anthony M. Musolf & Cristina M. Justice & Meng Yuan & Sahin Naqvi & Myoung Keun Lee & Dirk Vandermeulen & Heather L. Szabo-Rogers & Pau, 2023. "Joint multi-ancestry and admixed GWAS reveals the complex genetics behind human cranial vault shape," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    18. Yedael Y Waldman & Arjun Biddanda & Natalie R Davidson & Paul Billing-Ross & Maya Dubrovsky & Christopher L Campbell & Carole Oddoux & Eitan Friedman & Gil Atzmon & Eran Halperin & Harry Ostrer & Alon, 2016. "The Genetics of Bene Israel from India Reveals Both Substantial Jewish and Indian Ancestry," PLOS ONE, Public Library of Science, vol. 11(3), pages 1-28, March.
    19. Wang Chaolong & Szpiech Zachary A & Degnan James H & Jakobsson Mattias & Pemberton Trevor J & Hardy John A & Singleton Andrew B & Rosenberg Noah A, 2010. "Comparing Spatial Maps of Human Population-Genetic Variation Using Procrustes Analysis," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 9(1), pages 1-22, January.
    20. Zhaoming Wang & Allan Hildesheim & Sophia S Wang & Rolando Herrero & Paula Gonzalez & Laurie Burdette & Amy Hutchinson & Gilles Thomas & Stephen J Chanock & Kai Yu, 2010. "Genetic Admixture and Population Substructure in Guanacaste Costa Rica," PLOS ONE, Public Library of Science, vol. 5(10), pages 1-10, October.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49726-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.