Dissecting genetic and sex-specific sources of host heterogeneity in pathogen shedding and spread.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
Read Online Read More Add to Saved list
  • Author(s): Siva-Jothy JA;Siva-Jothy JA; Vale PF; Vale PF; Vale PF
  • Source:
    PLoS pathogens [PLoS Pathog] 2021 Jan 19; Vol. 17 (1), pp. e1009196. Date of Electronic Publication: 2021 Jan 19 (Print Publication: 2021).
  • Publication Type:
    Journal Article; Research Support, Non-U.S. Gov't
  • Language:
    English
  • Additional Information
    • Source:
      Publisher: Public Library of Science Country of Publication: United States NLM ID: 101238921 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7374 (Electronic) Linking ISSN: 15537366 NLM ISO Abbreviation: PLoS Pathog Subsets: MEDLINE
    • Publication Information:
      Original Publication: San Francisco, CA : Public Library of Science, c2005-
    • Subject Terms:
      Host-Pathogen Interactions* ; Viral Load* ; Virus Shedding*; Drosophila melanogaster/*genetics ; Drosophila melanogaster/*virology ; Insect Viruses/*pathogenicity; Animals ; Drosophila melanogaster/growth & development ; Female ; Longevity ; Male ; Sex Factors
    • Abstract:
      Host heterogeneity in disease transmission is widespread but precisely how different host traits drive this heterogeneity remains poorly understood. Part of the difficulty in linking individual variation to population-scale outcomes is that individual hosts can differ on multiple behavioral, physiological and immunological axes, which will together impact their transmission potential. Moreover, we lack well-characterized, empirical systems that enable the quantification of individual variation in key host traits, while also characterizing genetic or sex-based sources of such variation. Here we used Drosophila melanogaster and Drosophila C Virus as a host-pathogen model system to dissect the genetic and sex-specific sources of variation in multiple host traits that are central to pathogen transmission. Our findings show complex interactions between genetic background, sex, and female mating status accounting for a substantial proportion of variance in lifespan following infection, viral load, virus shedding, and viral load at death. Two notable findings include the interaction between genetic background and sex accounting for nearly 20% of the variance in viral load, and genetic background alone accounting for ~10% of the variance in viral shedding and in lifespan following infection. To understand how variation in these traits could generate heterogeneity in individual pathogen transmission potential, we combined measures of lifespan following infection, virus shedding, and previously published data on fly social aggregation. We found that the interaction between genetic background and sex explained ~12% of the variance in individual transmission potential. Our results highlight the importance of characterising the sources of variation in multiple host traits to understand the drivers of heterogeneity in disease transmission.
      Competing Interests: The authors have declared that no competing interests exist.
    • Comments:
      Erratum in: PLoS Pathog. 2021 Mar 8;17(3):e1009415. (PMID: 33684173)
    • References:
      Int J Parasitol Parasites Wildl. 2013 Sep 18;2:235-45. (PMID: 24533342)
      J Evol Biol. 2017 Jul;30(7):1325-1335. (PMID: 28425174)
      Proc Biol Sci. 2016 Apr 13;283(1828):. (PMID: 27053751)
      Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):338-42. (PMID: 8990210)
      Nat Commun. 2015 Jul 27;6:7829. (PMID: 26213329)
      PLoS Genet. 2012;8(11):e1003057. (PMID: 23166512)
      PLoS One. 2007 Aug 22;2(8):e747. (PMID: 17712403)
      Nat Rev Immunol. 2014 Dec;14(12):796-810. (PMID: 25421701)
      Parasitology. 2013 Jun;140(7):803-13. (PMID: 23425516)
      Trends Parasitol. 2016 May;32(5):356-367. (PMID: 26850821)
      J Insect Physiol. 2015 Nov;82:28-32. (PMID: 26301521)
      Int J Parasitol. 2003 Aug;33(9):909-17. (PMID: 12906875)
      Evolution. 2011 Aug;65(8):2325-34. (PMID: 21790578)
      Brain Behav Immun. 2008 Jul;22(5):676-89. (PMID: 17719201)
      Int J Infect Dis. 2011 Aug;15(8):e510-3. (PMID: 21737332)
      Proc Biol Sci. 2020 Nov 11;287(1938):20201653. (PMID: 33171094)
      Biol Rev Camb Philos Soc. 2017 Feb;92(1):551-571. (PMID: 26800512)
      Math Biosci. 2020 Mar;321:108294. (PMID: 31836567)
      Am Nat. 2015 Aug;186(2):252-63. (PMID: 26655153)
      Nat Commun. 2015 Jan 08;6:5975. (PMID: 25569306)
      Ecol Lett. 2013 Aug;16(8):975-84. (PMID: 23714379)
      Cell Host Microbe. 2015 Oct 14;18(4):398-401. (PMID: 26468744)
      Int J Parasitol. 2015 Jun;45(7):455-63. (PMID: 25812832)
      Int J Parasitol. 2009 Sep;39(11):1263-8. (PMID: 19397911)
      Sci Rep. 2019 Mar 20;9(1):4924. (PMID: 30894567)
      J R Soc Interface. 2012 Dec 19;10(80):20120588. (PMID: 23256186)
      Am J Epidemiol. 2013 Mar 1;177(5):474-86. (PMID: 23403987)
      Nat Rev Microbiol. 2008 Jun;6(6):477-87. (PMID: 18533288)
      Front Ecol Environ. 2012 Mar 1;10(2):75-82. (PMID: 23482675)
      Trends Ecol Evol. 2010 Jan;25(1):21-7. (PMID: 19782425)
      Nature. 2005 Nov 17;438(7066):355-9. (PMID: 16292310)
      J Exp Biol. 2013 Sep 1;216(Pt 17):3350-7. (PMID: 23685974)
      PLoS Biol. 2012;10(2):e1001271. (PMID: 22389630)
      Parasitology. 1995;111 Suppl:S111-27. (PMID: 8632918)
      PLoS One. 2010 Aug 26;5(8):e12421. (PMID: 20865043)
      Nature. 2014 Jul 10;511(7508):228-31. (PMID: 25008532)
      J Insect Physiol. 2013 Feb;59(2):130-7. (PMID: 23159523)
      Philos Trans R Soc Lond B Biol Sci. 2009 Jan 12;364(1513):15-26. (PMID: 18926975)
      J Anim Ecol. 2013 Sep;82(5):976-86. (PMID: 23734782)
      Proc Biol Sci. 2000 Aug 7;267(1452):1555-63. (PMID: 11007332)
      Biol Lett. 2013 Feb 13;9(2):20121145. (PMID: 23407498)
      Proc Biol Sci. 2016 Apr 27;283(1829):. (PMID: 27097926)
      Sci Rep. 2017 Apr 19;7(1):910. (PMID: 28424526)
      Int J Parasitol. 2011 Nov;41(13-14):1397-402. (PMID: 22056297)
      Biom J. 2008 Jun;50(3):346-63. (PMID: 18481363)
      PLoS Pathog. 2014 Dec 04;10(12):e1004507. (PMID: 25473839)
      J Virol. 2014 Dec;88(24):14057-69. (PMID: 25253354)
      J Insect Physiol. 2013 Oct;59(10):1024-30. (PMID: 23891750)
      Tuberculosis (Edinb). 2013 Jan;93(1):104-7. (PMID: 23219235)
      Cell. 1998 Sep 4;94(5):679-89. (PMID: 9741632)
      Biol Lett. 2019 Sep 27;15(9):20190344. (PMID: 31530113)
      Am J Epidemiol. 2004 Oct 15;160(8):719-28. (PMID: 15466494)
      Int J Environ Res Public Health. 2020 May 24;17(10):. (PMID: 32456346)
      Dis Model Mech. 2011 Jan;4(1):21-30. (PMID: 21183483)
      J Anim Ecol. 2014 Jan;83(1):256-65. (PMID: 23926945)
      Biol Lett. 2016 Jul;12(7):. (PMID: 27381885)
      Biol Lett. 2019 Nov 29;15(11):20190557. (PMID: 31744410)
      Am Nat. 2011 Apr;177(4):510-21. (PMID: 21460572)
      Trends Parasitol. 2015 Sep;31(9):419-25. (PMID: 26048486)
      Behav Ecol. 2018 Nov-Dec;29(6):1426-1435. (PMID: 30510395)
      MMWR Morb Mortal Wkly Rep. 2003 May 9;52(18):405-11. (PMID: 12807088)
      PLoS Biol. 2015 Jul 14;13(7):e1002210. (PMID: 26172158)
      Ann Gastroenterol. 2013;26(2):132-134. (PMID: 24714738)
      Int J Parasitol. 2016 Feb;46(2):123-31. (PMID: 26552016)
    • Publication Date:
      Date Created: 20210119 Date Completed: 20210426 Latest Revision: 20230919
    • Publication Date:
      20240105
    • Accession Number:
      PMC7846003
    • Accession Number:
      10.1371/journal.ppat.1009196
    • Accession Number:
      33465160