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Strong positive selection biases identity-by-descent-based inferences of recent demography and population structure in Plasmodium falciparum

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Listed:
  • Bing Guo

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Victor Borda

    (University of Maryland School of Medicine)

  • Roland Laboulaye

    (University of Maryland School of Medicine)

  • Michele D. Spring

    (Armed Forces Research Institute of Medical Sciences)

  • Mariusz Wojnarski

    (Armed Forces Research Institute of Medical Sciences)

  • Brian A. Vesely

    (Armed Forces Research Institute of Medical Sciences)

  • Joana C. Silva

    (University of Maryland School of Medicine
    University of Maryland School of Medicine
    Universidade NOVA de Lisboa (NOVA))

  • Norman C. Waters

    (Armed Forces Research Institute of Medical Sciences)

  • Timothy D. O’Connor

    (University of Maryland School of Medicine)

  • Shannon Takala-Harrison

    (University of Maryland School of Medicine)

Abstract

Malaria genomic surveillance often estimates parasite genetic relatedness using metrics such as Identity-By-Decent (IBD), yet strong positive selection stemming from antimalarial drug resistance or other interventions may bias IBD-based estimates. In this study, we use simulations, a true IBD inference algorithm, and empirical data sets from different malaria transmission settings to investigate the extent of this bias and explore potential correction strategies. We analyze whole genome sequence data generated from 640 new and 3089 publicly available Plasmodium falciparum clinical isolates. We demonstrate that positive selection distorts IBD distributions, leading to underestimated effective population size and blurred population structure. Additionally, we discover that the removal of IBD peak regions partially restores the accuracy of IBD-based inferences, with this effect contingent on the population’s background genetic relatedness and extent of inbreeding. Consequently, we advocate for selection correction for parasite populations undergoing strong, recent positive selection, particularly in high malaria transmission settings.

Suggested Citation

  • Bing Guo & Victor Borda & Roland Laboulaye & Michele D. Spring & Mariusz Wojnarski & Brian A. Vesely & Joana C. Silva & Norman C. Waters & Timothy D. O’Connor & Shannon Takala-Harrison, 2024. "Strong positive selection biases identity-by-descent-based inferences of recent demography and population structure in Plasmodium falciparum," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46659-0
    DOI: 10.1038/s41467-024-46659-0
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    1. Eunjung Han & Peter Carbonetto & Ross E. Curtis & Yong Wang & Julie M. Granka & Jake Byrnes & Keith Noto & Amir R. Kermany & Natalie M. Myres & Mathew J. Barber & Kristin A. Rand & Shiya Song & Theodo, 2017. "Clustering of 770,000 genomes reveals post-colonial population structure of North America," Nature Communications, Nature, vol. 8(1), pages 1-12, April.
    2. Lawrence Hubert & Phipps Arabie, 1985. "Comparing partitions," Journal of Classification, Springer;The Classification Society, vol. 2(1), pages 193-218, December.
    3. John C. Wootton & Xiaorong Feng & Michael T. Ferdig & Roland A. Cooper & Jianbing Mu & Dror I. Baruch & Alan J. Magill & Xin-zhuan Su, 2002. "Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum," Nature, Nature, vol. 418(6895), pages 320-323, July.
    4. Juba Nait Saada & Georgios Kalantzis & Derek Shyr & Fergus Cooper & Martin Robinson & Alexander Gusev & Pier Francesco Palamara, 2020. "Identity-by-descent detection across 487,409 British samples reveals fine scale population structure and ultra-rare variant associations," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    5. Jonathan Kim & Yong Zi Tan & Kathryn J. Wicht & Satchal K. Erramilli & Satish K. Dhingra & John Okombo & Jeremie Vendome & Laura M. Hagenah & Sabrina I. Giacometti & Audrey L. Warren & Kamil Nosol & P, 2019. "Structure and drug resistance of the Plasmodium falciparum transporter PfCRT," Nature, Nature, vol. 576(7786), pages 315-320, December.
    6. Jerome Kelleher & Kevin R Thornton & Jaime Ashander & Peter L Ralph, 2018. "Efficient pedigree recording for fast population genetics simulation," PLOS Computational Biology, Public Library of Science, vol. 14(11), pages 1-21, November.
    7. Gabrielle A. Josling & Timothy J. Russell & Jarrett Venezia & Lindsey Orchard & Riëtte Biljon & Heather J. Painter & Manuel Llinás, 2020. "Dissecting the role of PfAP2-G in malaria gametocytogenesis," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    8. Romain Fournier & Zoi Tsangalidou & David Reich & Pier Francesco Palamara, 2023. "Haplotype-based inference of recent effective population size in modern and ancient DNA samples," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. Amol C. Shetty & Christopher G. Jacob & Fang Huang & Yao Li & Sonia Agrawal & David L. Saunders & Chanthap Lon & Mark M. Fukuda & Pascal Ringwald & Elizabeth A. Ashley & Kay Thwe Han & Tin Maung Hlain, 2019. "Genomic structure and diversity of Plasmodium falciparum in Southeast Asia reveal recent parasite migration patterns," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    10. Pardis C. Sabeti & David E. Reich & John M. Higgins & Haninah Z. P. Levine & Daniel J. Richter & Stephen F. Schaffner & Stacey B. Gabriel & Jill V. Platko & Nick J. Patterson & Gavin J. McDonald & Han, 2002. "Detecting recent positive selection in the human genome from haplotype structure," Nature, Nature, vol. 419(6909), pages 832-837, October.
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