Section: Evolutionary Biology
Topic: Evolution, Microbiology

Heterogeneities in infection outcomes across species: sex and tissue differences in virus susceptibility

10.24072/pcjournal.242 - Peer Community Journal, Volume 3 (2023), article no. e16.

Get full text PDF Peer reviewed and recommended by PCI

Species vary in their susceptibility to pathogens, and this can alter the ability of a pathogen to infect a novel host. However, many factors can generate heterogeneity in infection outcomes, obscuring our ability to understand pathogen emergence. Such heterogeneities can alter the consistency of responses across individuals and host species. For example, sexual dimorphism in susceptibility means males are often intrinsically more susceptible than females (although this can vary by host and pathogen). Further, we know little about whether the tissues infected by a pathogen in one host are the same in another species, and how this relates to the harm a pathogen does to its host. Here, we first take a comparative approach to examine sex differences in susceptibility across 31 species of Drosophilidae infected with Drosophila C Virus (DCV). We found a strong positive inter-specific correlation in viral load between males and females, with a close to 1:1 relationship, suggesting that susceptibility to DCV across species is not sex specific. Next, we made comparisons of the tissue tropism of DCV across seven species of fly. We found differences in viral load between the tissues of the seven host species, but no evidence of tissues showing different patterns of susceptibility in different host species. We conclude that, in this system, patterns of viral infectivity across host species are robust between males and females, and susceptibility in a given host is general across tissue types.

Published online:
DOI: 10.24072/pcjournal.242
Type: Research article
Roberts, Katherine E 1; Longdon, Ben 1

1 Centre for Ecology and Conservation, University of Exeter, Penryn Campus, TR10 9FE, UK
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Roberts, Katherine E and Longdon, Ben},
     title = {Heterogeneities in infection outcomes across species: sex and tissue differences in virus susceptibility},
     journal = {Peer Community Journal},
     eid = {e16},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.242},
     url = {}
AU  - Roberts, Katherine E
AU  - Longdon, Ben
TI  - Heterogeneities in infection outcomes across species: sex and tissue differences in virus susceptibility
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.242
ID  - 10_24072_pcjournal_242
ER  - 
%0 Journal Article
%A Roberts, Katherine E
%A Longdon, Ben
%T Heterogeneities in infection outcomes across species: sex and tissue differences in virus susceptibility
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%R 10.24072/pcjournal.242
%F 10_24072_pcjournal_242
Roberts, Katherine E; Longdon, Ben. Heterogeneities in infection outcomes across species: sex and tissue differences in virus susceptibility. Peer Community Journal, Volume 3 (2023), article  no. e16. doi : 10.24072/pcjournal.242.

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100638

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Abate, B. B.; Kassie, A. M.; Kassaw, M. W.; Aragie, T. G.; Masresha, S. A. Sex difference in coronavirus disease (COVID-19): a systematic review and meta-analysis, BMJ Open, Volume 10 (2020) no. 10 | DOI

[2] Ashby, B.; Jones, J. E.; Knell, R. J.; Hurst, G. D. Sexually transmitted infections in natural populations: what have we learnt from beetles and beyond?, Wildlife Disease Ecology, Cambridge University Press, 2019, pp. 187-222 | DOI

[3] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using lme4, Journal of Statistical Software, Volume 67 (2015) no. 1 | DOI

[4] Belmonte, R. L.; Corbally, M.-K.; Duneau, D. F.; Regan, J. C. Sexual Dimorphisms in Innate Immunity and Responses to Infection in Drosophila melanogaster, Frontiers in Immunology, Volume 10 (2020) | DOI

[5] Brierley, L.; Pedersen, A. B.; Woolhouse, M. E. J. Tissue tropism and transmission ecology predict virulence of human RNA viruses, PLOS Biology, Volume 17 (2019) no. 11 | DOI

[6] Chtarbanova, S.; Lamiable, O.; Lee, K.-Z.; Galiana, D.; Troxler, L.; Meignin, C.; Hetru, C.; Hoffmann, J. A.; Daeffler, L.; Imler, J.-L. Drosophila C Virus Systemic Infection Leads to Intestinal Obstruction, Journal of Virology, Volume 88 (2014) no. 24, pp. 14057-14069 | DOI

[7] Drummond, A. J.; Suchard, M. A.; Xie, D.; Rambaut, A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7, Molecular Biology and Evolution, Volume 29 (2012) no. 8, pp. 1969-1973 | DOI

[8] Faria, N. R.; Suchard, M. A.; Rambaut, A.; Streicker, D. G.; Lemey, P. Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 368 (2013) no. 1614 | DOI

[9] Farrell, M. J.; Davies, T. J. Disease mortality in domesticated animals is predicted by host evolutionary relationships, Proceedings of the National Academy of Sciences, Volume 116 (2019) no. 16, pp. 7911-7915 | DOI

[10] Ferreira, Á. G.; Naylor, H.; Esteves, S. S.; Pais, I. S.; Martins, N. E.; Teixeira, L. The Toll-Dorsal Pathway Is Required for Resistance to Viral Oral Infection in Drosophila, PLoS Pathogens, Volume 10 (2014) no. 12 | DOI

[11] Gilbert, G. S.; Webb, C. O. Phylogenetic signal in plant pathogen–host range, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 12, pp. 4979-4983 | DOI

[12] Gupta, V.; Stewart, C. O.; Rund, S. S. C.; Monteith, K.; Vale, P. F. Costs and benefits of sublethal Drosophila C virus infection, Journal of Evolutionary Biology, Volume 30 (2017) no. 7, pp. 1325-1335 | DOI

[13] Guth, S.; Visher, E.; Boots, M.; Brook, C. E. Host phylogenetic distance drives trends in virus virulence and transmissibility across the animal–human interface, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 374 (2019) no. 1782 | DOI

[14] Hadfield, J. D. MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package, Journal of Statistical Software, Volume 33 (2010) no. 2 | DOI

[15] Housworth, E. A.; Martins, E. P.; Lynch, M. The Phylogenetic Mixed Model, The American Naturalist, Volume 163 (2004) no. 1, pp. 84-96 | DOI

[16] Imrie, R. M.; Roberts, K. E.; Longdon, B. Between virus correlations in the outcome of infection across host species: evidence of virus genotype by host species interactions | DOI

[17] Jousset FX; Plus N; Croizier G; Thomas M [Existence in Drosophila of 2 groups of picornavirus with different biological and serological properties], C R Acad Sci Hebd Seances Acad Sci D, Volume 275 (1972), pp. 3043-3046

[18] Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; Thierer, T.; Ashton, B.; Meintjes, P.; Drummond, A. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data, Bioinformatics, Volume 28 (2012) no. 12, pp. 1647-1649 | DOI

[19] Kellermann, V.; Overgaard, J.; Sgrò, C. M.; Hoffmann, A. A. Phylogenetic and environmental patterns of sex differentiation in physiological traits across Drosophila species, Journal of Evolutionary Biology, Volume 35 (2022) no. 11, pp. 1548-1557 | DOI

[20] Kelly, C. D.; Stoehr, A. M.; Nunn, C.; Smyth, K. N.; Prokop, Z. M. Sexual dimorphism in immunity across animals: a meta‐analysis, Ecology Letters, Volume 21 (2018) no. 12, pp. 1885-1894 | DOI

[21] Kitchen, A.; Shackelton, L. A.; Holmes, E. C. Family level phylogenies reveal modes of macroevolution in RNA viruses, Proceedings of the National Academy of Sciences, Volume 108 (2010) no. 1, pp. 238-243 | DOI

[22] Knell, R. J.; Mary Webberley, K. Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour, Biological Reviews, Volume 79 (2004) no. 3, pp. 557-581 | DOI

[23] Lazzaro, B. P.; Little, T. J. Immunity in a variable world, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 364 (2008) no. 1513, pp. 15-26 | DOI

[24] Levin, B. R.; Bull, J. J. Short-sighted evolution and the virulence of pathogenic microorganisms, Trends in Microbiology, Volume 2 (1994) no. 3, pp. 76-81 | DOI

[25] Lockhart, A. B.; Thrall, P. H.; Antonovics, J. Sexually transmitted diseases in animals: ecological and evolutionary implications, Biological Reviews, Volume 71 (1996) no. 3, pp. 415-471 | DOI

[26] Longdon, B.; Brockhurst, M. A.; Russell, C. A.; Welch, J. J.; Jiggins, F. M. The Evolution and Genetics of Virus Host Shifts, PLoS Pathogens, Volume 10 (2014) no. 11 | DOI

[27] Longdon, B.; Cao, C.; Martinez, J.; Jiggins, F. M. Previous Exposure to an RNA Virus Does Not Protect against Subsequent Infection in Drosophila melanogaster, PLoS ONE, Volume 8 (2013) no. 9 | DOI

[28] Longdon, B.; Day, J. P.; Alves, J. M.; Smith, S. C. L.; Houslay, T. M.; McGonigle, J. E.; Tagliaferri, L.; Jiggins, F. M. Host shifts result in parallel genetic changes when viruses evolve in closely related species, PLOS Pathogens, Volume 14 (2018) no. 4 | DOI

[29] Longdon, B.; Hadfield, J. D.; Day, J. P.; Smith, S. C. L.; McGonigle, J. E.; Cogni, R.; Cao, C.; Jiggins, F. M. The Causes and Consequences of Changes in Virulence following Pathogen Host Shifts, PLOS Pathogens, Volume 11 (2015) no. 3 | DOI

[30] Longdon, B.; Hadfield, J. D.; Webster, C. L.; Obbard, D. J.; Jiggins, F. M. Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts, PLoS Pathogens, Volume 7 (2011) no. 9 | DOI

[31] Martel, A.; Blooi, M.; Adriaensen, C.; Van Rooij, P.; Beukema, W.; Fisher, M. C.; Farrer, R. A.; Schmidt, B. R.; Tobler, U.; Goka, K.; Lips, K. R.; Muletz, C.; Zamudio, K. R.; Bosch, J.; Lotters, S.; Wombwell, E.; Garner, T. W. J.; Cunningham, A. A.; Spitzen-van der Sluijs, A.; Salvidio, S.; Ducatelle, R.; Nishikawa, K.; Nguyen, T. T.; Kolby, J. E.; Van Bocxlaer, I.; Bossuyt, F.; Pasmans, F. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders, Science, Volume 346 (2014) no. 6209, pp. 630-631 | DOI

[32] McCall, L.-I. Quo vadis? Central Rules of Pathogen and Disease Tropism, Frontiers in Cellular and Infection Microbiology, Volume 11 (2021) | DOI

[33] Mollentze, N.; Keen, D.; Munkhbayar, U.; Biek, R.; Streicker, D. G. Variation in the ACE2 receptor has limited utility for SARS-CoV-2 host prediction | DOI

[34] Mollentze, N.; Streicker, D. G.; Murcia, P. R.; Hampson, K.; Biek, R. Virulence mismatches in index hosts shape the outcomes of cross-species transmission, Proceedings of the National Academy of Sciences, Volume 117 (2020) no. 46, pp. 28859-28866 | DOI

[35] Moore, S. L.; Wilson, K. Parasites as a Viability Cost of Sexual Selection in Natural Populations of Mammals, Science, Volume 297 (2002) no. 5589, pp. 2015-2018 | DOI

[36] Nunn, C. L.; Lindenfors, P.; Pursall, E. R.; Rolff, J. On sexual dimorphism in immune function, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 364 (2008) no. 1513, pp. 61-69 | DOI

[37] Pagel, M. Inferring the historical patterns of biological evolution, Nature, Volume 401 (1999) no. 6756, pp. 877-884 | DOI

[38] Poulin, R. Sexual Inequalities in Helminth Infections: A Cost of Being a Male?, The American Naturalist, Volume 147 (1996) no. 2, pp. 287-295 | DOI

[39] Regan, J. C.; Partridge, L. Gender and longevity: Why do men die earlier than women? Comparative and experimental evidence, Best Practice & Research Clinical Endocrinology & Metabolism, Volume 27 (2013) no. 4, pp. 467-479 | DOI

[40] Roberts, K. E.; Hadfield, J. D.; Sharma, M. D.; Longdon, B. Changes in temperature alter the potential outcomes of virus host shifts, PLOS Pathogens, Volume 14 (2018) no. 10 | DOI

[41] Roberts, K. E.; Longdon, B. Viral susceptibility across host species is largely independent of dietary protein to carbohydrate ratios, Journal of Evolutionary Biology, Volume 34 (2021) no. 5, pp. 746-756 | DOI

[42] Rolff, J. Bateman's principle and immunity, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 269 (2002) no. 1493, pp. 867-872 | DOI

[43] Sheridan, L. A. D.; Poulin, R.; Ward, D. F.; Zuk, M. Sex differences in parasitic infections among arthropod hosts: is there a male bias?, Oikos, Volume 88 (2000) no. 2, pp. 327-334 | DOI

[44] Siva-Jothy, J. A.; Vale, P. F. Dissecting genetic and sex-specific sources of host heterogeneity in pathogen shedding and spread, PLOS Pathogens, Volume 17 (2021) no. 1 | DOI

[45] Taber, S. W.; Pease, C. M. Paramyxovirus Phylogeny: Tissue Tropism Evolves Slower than Host Specificity, Evolution, Volume 44 (1990) no. 2 | DOI

[46] R Core Team R: a language and environment for statistical computing. V 2.4. R Foundation for Statistical Computing, Vienna, Austria., 2006

[47] Vale, P. F.; Jardine, M. D. Infection avoidance behavior: Viral exposure reduces the motivation to forage in female Drosophila melanogaster, Fly, Volume 11 (2016) no. 1, pp. 3-9 | DOI

[48] vom Steeg, L. G.; Klein, S. L. SeXX Matters in Infectious Disease Pathogenesis, PLOS Pathogens, Volume 12 (2016) no. 2 | DOI

[49] Warren, C. J.; Meyerson, N. R.; Dirasantha, O.; Feldman, E. R.; Wilkerson, G. K.; Sawyer, S. L. Selective use of primate CD4 receptors by HIV-1, PLOS Biology, Volume 17 (2019) no. 6 | DOI

[50] Wilson, K.; Cotter, S. C. Host–Parasite Interactions and the Evolution of Immune Defense, Advances in the Study of Behavior, Elsevier, 2013, pp. 81-174 | DOI

[51] Yeates, D.; Hastings, A. Anatomical Atlas of the male Drosophila melanogaster. CSIRO.

Cited by Sources: