Abstract
Scientists have described thousands of species of viruses, many of which are pathogens of vertebrates. Given that vertebrates have their highly sophisticated adaptive immune systems capable of memorizing pathogens, interaction with such systems should theoretically be one of the most important factors influencing the evolution of viruses. The review focuses on how acquired immunity (infection-induced and vaccine-induced) affects the most important medical characteristics of viral pathogens—transmissibility, infectivity, and virulence. Both known real examples of the evolution of viruses in immunized populations and theoretical articles and the results of mathematical modeling are considered. Special attention is paid to the SARS-CoV-2 pandemic. Methodological recommendations are given for creating vaccines and conducting vaccination campaigns in the light of the raised evolutionary issues.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1134%2FS2079086424010079/MediaObjects/13335_2024_1352_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1134%2FS2079086424010079/MediaObjects/13335_2024_1352_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1134%2FS2079086424010079/MediaObjects/13335_2024_1352_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1134%2FS2079086424010079/MediaObjects/13335_2024_1352_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1134%2FS2079086424010079/MediaObjects/13335_2024_1352_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1134%2FS2079086424010079/MediaObjects/13335_2024_1352_Fig6_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1134%2FS2079086424010079/MediaObjects/13335_2024_1352_Fig7_HTML.png)
REFERENCES
André, J.-B. and Gandon, S., Vaccination, within-host dynamics, and virulence evolution, Evolution, 2006, vol. 60, no. 1, pp. 13–23. https://doi.org/10.1111/j.0014-3820.2006.tb01077.x
Andreano, E., Piccini, G., Licastro, D., Casalino, L., Johnson, N.V., et al., SARS-CoV-2 escape from a highly neutralizing COVID-19 convalescent plasma, Proc. Natl Acad. Sci. USA, 2021, vol. 118, no. 36, p. e2103154118. https://doi.org/10.1073/pnas.2103154118
Antoulas, A.C., Approximation of large-scale dynamical systems: An overview, IFAC Proceedings Volumes, 2004, vol. 37, no. 11, pp. 19–28. https://doi.org/10.1016/s1474-6670(17)31584-7
Arora, S., Grover, V., Saluja, P., Algarni, Y.A., Saquib, S.A., et al., Literature review of Omicron: A grim reality amidst COVID-19, Microorganisms, 2022, vol. 10, no. 2, p. 451. https://doi.org/10.3390/microorganisms10020451
Aviagen, Marek’s Disease Virus, 2017. https://en.aviagen.com/assets/Tech_Center/Broiler_Breeder_Tech_ Articles/English/MareksDiseaseVirus-2017-EN.pdf.
Butt, A.A., Dargham, S.R., Loka, S., Shaik, R.M., Chemaitelly, H., et al., COVID-19 disease severity in children infected with the Omicron variant, Clin. Infect. Dis., 2022, vol. 75, no. 1, pp. e361–e367. https://doi.org/10.1093/cid/ciac275
Cecchinato, M., Catelli, E., Lupini, C., Ricchizzi, E., Clubbe, J., et al., Avian metapneumovirus (AMPV) attachment protein involvement in probable virus evolution concurrent with mass live vaccine introduction, Vet. Microbiol., 2010, vol. 146, no. 1–2, pp. 24–34. https://doi.org/10.1016/j.vetmic.2010.04.014
Cele, S., Karim, F., Lustig, G., San, J.E., Hermanus, T., et al., SARS-CoV-2 prolonged infection during advanced HIV disease evolves extensive immune escape, Cell Host Microbe, 2022, vol. 30, no. 2, pp. 154–162. https://doi.org/10.1016/j.chom.2022.01.005
Chinesta, F., Huerta, A., Rozza, G., and Wilcox, K., Model reduction methods, in Encyclopedia of Computational Mechanics Second Edition, Stein, E., Borst, R., and Hughes, T.J.R., Eds., Hoboken: Wiley, 2017. https://doi.org/10.1002/9781119176817.ecm2110
Cloete, J., Kruger, A., Masha, M., Du Plessis, N.M., Mawela, D., et al., Paediatric hospitalisations due to COVID-19 during the first SARS-CoV-2 omicron (B.1.1.529) variant wave in South Africa: A multicentre observational study, Lancet Child Adolesc. Health, 2022, vol. 6, no. 5, pp. 294–302. https://doi.org/10.1016/S2352-4642(22)00027-X
Coyne, K.P., Reed, F.C., Porter, C.J., Dawson, S., Gaskell, R.M., and Radford, A.D., Recombination of Feline calicivirus within an endemically infected cat colony, J. Gen. Virol., 2006, vol. 87, no. 4, pp. 921–926. https://doi.org/10.1099/vir.0.81537-0
Crépey, P., Noël, H., and Alizon, S., Challenges for mathematical epidemiological modelling, Anaesthesia Critical Care Pain Med., 2022, vol. 41, no. 2, p. 101053. https://doi.org/10.1016/j.accpm.2022.101053
Davison, F. and Nair, V., Marek’s Disease: An Evolving Problem, Amsterdam: Elsevier, 2004.
Day, T., Parasite transmission modes and the evolution of virulence, Evolution, 2001, vol. 55, pp. 2389–2400. https://doi.org/10.1111/j.0014-3820.2001.tb00754.x
Dimmock, N.J., Easton, A.J., and Leppard, K.N., Introduction to Modern Virology, Malden: Blackwell Publishing, 2007, 6th ed.
Du, X., Tang, H., Gao, L., Wu, Z., Meng, F., et al., Omicron adopts a different strategy from Delta and other variants to adapt to host, Signal Transduction Targeted Ther., 2022, vol. 7, no. 1, p. 45. https://doi.org/10.1038/s41392-022-00903-5
Egeren, D. van, Novokhodko, A., Stoddard, M., Tran, U., Zetter, B., et al., Risk of rapid evolutionary escape from biomedical interventions targeting SARS-CoV-2 spike protein, PLoS One, 2021, vol. 16, no. 4, p. e0250780. https://doi.org/10.1371/journal.pone.0250780
El-Diwany, R., Cohen, V.J., Mankowski, M.C., Wasilewski, L.N., Brady, J.K., et al., Extra-epitopic hepatitis C virus polymorphisms confer resistance to broadly neutralizing antibodies by modulating binding to scavenger receptor B1, PLoS Pathog., 2017, vol. 13, no. 2, p. e1006235. https://doi.org/10.1371/journal.ppat.1006235
Ewald, P.W., Transmission modes and the evolution of virulence, Human Nature, 1991, vol. 2, pp. 1–30. https://doi.org/10.1007/BF02692179
Ewald, P.W., The evolution of virulence, Sci. Am., 1993, vol. 268, no. 4, pp. 86–93. http://www.jstor.org/stable/24941444.
Franceschi, C., Valensin, S., Fagnoni, F., Barbi, C., and Bonafè, M., Biomarkers of immunosenescence within an evolutionary perspective: The challenge of heterogeneity and the role of antigenic load, Exp. Gerontol., 1999, vol. 34, no. 8, pp. 911–921. https://doi.org/10.1016/S0531-5565(99)00068-6
Franzo, G., Tucciarone, C., Cecchinato, M., and Drigo, M., Porcine circovirus type 2 (PCV2) evolution before and after the vaccination introduction: A large scale epidemiological study, Sci. Rep., 2016, vol. 6. https://doi.org/10.1038/srep39458
Franzo, G., Legnardi, M., Tucciarone, C.M., Drigo, M., Martini, M., and Cecchinato, M., Evolution of infectious bronchitis virus in the field after homologous vaccination introduction, Vet. Res., 2019, vol. 50, p. 92. https://doi.org/10.1186/s13567-019-0713-4
Frasca, D., Reidy, L., Romero, M., Diaz, A., Cray, C., et al., The majority of SARS-CoV-2-specific antibodies in COVID-19 patients with obesity are autoimmune and not neutralizing, Int. J. Obes., 2022, vol. 46, pp. 427–432. https://doi.org/10.1038/s41366-021-01016-9
Garcia-Beltran, W.F., Lam, E.C., St Denis, K., Nitido, A.D., Garcia, Z.H., et al., Multiple SARS-CoV-2 variants escape neutralization by vaccine-induced humoral immunity, Cell, 2021, vol. 184, no. 9, pp. 2372–2383. https://doi.org/10.1016/j.cell.2021.03.013
Ghosh, D., Bernstein, J.A., and Mersha, T.B., COVID-19 pandemic: The African paradox, J. Global Health, 2020, vol. 10, no. 2, p. 020348. https://doi.org/10.7189/jogh.10.020348
Ginaldi, L., Martinis, M. de, Monti, D., and Franceschi, C., Chronic antigenic load and apoptosis in immunosenescence, Trends Immunol., 2005, vol. 26, no. 2, pp. 79–84. https://doi.org/10.1016/j.it.2004.11.005
Grabowski, F., Kochańczyk, M., and Lipniacki, T., The spread of SARS-CoV-2 variant Omicron with a doubling time of 2.0–3.3 days can be explained by immune evasion, Viruses, 2022, vol. 14, no. 2, p. 294. https://doi.org/10.3390/v14020294
Grenfell, B.T., Pybus, O.G., Gog, J.R., Wood, J.L.N., Daly, J.M., et al., Unifying the epidemiological and evolutionary dynamics of pathogens, Science, 2004, vol. 303, no. 5656, pp. 327–332.
Hie, B., Zhong, E.D., Berger, B., and Bryson, B., Learning the language of viral evolution and escape, Science, 2021, vol. 371, no. 6526, pp. 284–288. https://doi.org/10.1126/science.abd7331
Hoffman, S.A., Costales, C., Sahoo, M.K., Palanisamy, S., Yamamoto, F., et al., SARS-CoV-2 neutralization resistance mutations in patient with HIV/AIDS, California, USA, Emerging Infect. Dis., 2021, vol. 27, no. 10, pp. 2720−2723. https://doi.org/10.3201/eid2710.211461
Hui, K.P.Y., Ho, J.C.W., Cheung, M.C., Ng, K.C., Ching, R.H.H., et al., SARS-CoV-2 Omicron variant replication in human bronchus and lung ex vivo, Nature, 2022, vol. 603, no. 7902, pp. 715−720. https://doi.org/10.1038/s41586-022-04479-6
Jackson, B., Boni, M.F., Bull, M.J., Colleran, A., Colquhoun, R.M., et al., Generation and transmission of interlineage recombinants in the SARS-CoV-2 pandemic, Cell, 2021, vol. 184, no. 20, pp. 5179−5188. https://doi.org/10.1016/j.cell.2021.08.014
Jacobson, K.B., Pinsky, B.A., Rath, M.E.M., Wang, H., Miller, J.A., et al., Post-vaccination SARS-CoV-2 infections and incidence of the B.1.427/B.1.429 variant among healthcare personnel at a northern California academic medical center, medRxiv, 2021. https://doi.org/10.1101/2021.04.14.21255431
Kemp, S.A., Collier, D.A., Datir, R.P., Ferreira, I.A.T.M., Gayed, S., et al., SARS-CoV-2 evolution during treatment of chronic infection, Nature, 2021, vol. 592, no. 7853, pp. 277−282. https://doi.org/10.1038/s41586-021-03291-y
Kennedy, D.A. and Read, A.F., Why does drug resistance readily evolve but vaccine resistance does not?, Proc. R. Soc. B., 2017, vol. 284, no. 1851. https://doi.org/10.1098/rspb.2016.2562
Kostoff, R.N., Kanduc, D., Porter, A.L., Shoenfeld, Y., and Briggs, M.B., COVID-19 Vaccine Safety Considerations, Atlanta: Georgia Institute of Technology, 2020. http://hdl.handle.net/1853/63710
Lai, M.M.C., Recombination in large RNA viruses: Coronaviruses, Semin. Virol., 1996, vol. 7, no. 6, pp. 381−388. https://doi.org/10.1006/smvy.1996.0046
Legnardi, M., Tucciarone, C.M., Franzo, G., and Cecchinato, M., Infectious bronchitis virus evolution, diagnosis and control, Vet. Sci., 2020, vol. 7, no. 2, p. 79. https://doi.org/10.3390/vetsci7020079
Liu, J.L. and Kung, H.J., Marek’s disease herpesvirus transforming protein MEQ: A c-Jun analogue with an alternative life style, Virus Genes, 2000, vol. 21, nos. 1–2, pp. 51−64.
Liu, Q., Zhou, Y.H., and Yang, Z.Q., The cytokine storm of severe influenza and development of immunomodulatory therapy, Cell. Mol. Immunol., 2016, vol. 13, no. 1, pp. 3–10. https://doi.org/10.1038/cmi.2015.74
Marakasova, E., Baranova, A., and Pirofski, L., MMR vaccine and COVID-19: Measles protein homology may contribute to cross-reactivity or to complement activation protection, mBio, 2021, vol. 12, no. 1. https://doi.org/10.1128/mBio.03447-20
McMillan, P., Dexhiemer, T., Neubig, R.R., and Uhal, B.D., COVID-19—A theory of autoimmunity against ACE-2 explained, Front. Immunol., 2021, vol. 12, p. 582166. https://doi.org/10.3389/fimmu.2021.582166
Mlcochova, P., Kemp, S.A., Dhar, M.S., Papa, G., Meng, B., et al., SARS-CoV-2 B.1.617.2 Delta variant replication and immune evasion, Nature, 2021, vol. 599, pp. 114–119. https://doi.org/10.1038/s41586-021-03944-y
Morán Blanco, J.I., Alvarenga Bonilla, J.A., Homma, S., Suzuki, K., Fremont-Smith, P., and Villar Gómez de las Heras, K., Antihistamines and azithromycin as a treatment for COVID-19 on primary health care—A retrospective observational study in elderly patients, Pulm. Pharmacol. Ther., 2021, vol. 67, p. 101989. https://doi.org/10.1016/j.pupt.2021.101989
Ossiboff, R.J., Sheh, A., Shotton, J., Pesavento, P.A., and Parker, J.S.L., Feline caliciviruses (FCVs) isolated from cats with virulent systemic disease possess in vitro phenotypes distinct from those of other FCV isolates, J. Gen. Virol., 2007, vol. 88, no. 2, pp. 506−517. https://doi.org/10.1099/vir.0.82488-0
Plans Rubió, P., Is the basic reproductive number (R0) for measles viruses observed in recent outbreaks lower than in the pre-vaccination era?, Eurosurveillance, 2012, vol. 17, no. 31, p. 20233. https://doi.org/10.2807/ese.17.31.20233-en
Radford, A.D., Dawson, S., Coyne, K.P., Porter, C.J., and Gaskell, R.M., The challenge for the next generation of feline calicivirus vaccines, Vet. Microbiol., 2006, vol. 117, no. 1, pp. 14–18. https://doi.org/10.1016/j.vetmic.2006.04.004
Radford, A.D., Coyne, K.P., Dawson, S., Porter, C.J., and Gaskell, R.M., Feline calicivirus, Vet. Res., 2007, vol. 38, no. 2, pp. 319−335. https://doi.org/10.1051/vetres:2006056
Ragia, G. and Manolopoulos, V.G., Inhibition of SARS-CoV-2 entry through the ACE2/TMPRSS2 pathway: A promising approach for uncovering early COVID-19 drug therapies, Eur. J. Clin. Pharmacol., 2020, vol. 76, pp. 1623–1630. https://doi.org/10.1007/s00228-020-02963-4
Read, A.F., Pathogen evolution in a vaccinated world, 2016. https://www.youtube.com/watch?v=TeyxhehhEuo.
Read, A.F., Baigent, S.J., Powers, C., Kgosana, L.B., Blackwell, L., et al., Imperfect vaccination can enhance the transmission of highly virulent pathogens, PLoS Biol., 2015, vol. 13, no. 7, p. e1002198. https://doi.org/10.1371/journal.pbio.1002198
Sasaki, A., Lion, S., and Boots, M., Antigenic escape selects for the evolution of higher pathogen transmission and virulence, Nat. Ecol. Evol., 2022, vol. 6, pp. 51–62. https://doi.org/10.1038/s41559-021-01603-z
Scudellari, M., How the coronavirus infects cells—and why Delta is so dangerous, Nature News Feature, 2021. https://www.nature.com/articles/d41586-021-02039-y.
Shamblin, C.E., Greene, N., Arumugaswami, V., Dienglewicz, R.L., and Parcells, M.S., Comparative analysis of Marek’s disease virus (MDV) glycoprotein-, lytic antigen pp38- and transformation antigen Meq-encoding genes: Association of meq mutations with MDVs of high virulence, Vet. Microbiol., 2004, vol. 102, nos. 3–4, pp. 147−167. https://doi.org/10.1016/j.vetmic.2004.06.007
Sharif-Askari, N.S., Sharif-Askari, F.S., Alabed, M., Temsah, M., Heialy, S.A., et al., Airways expression of SARS-CoV-2 receptor, ACE2, and TMPRSS2 is lower in children than adults and increases with smoking and COPD, Mol. Ther.—Methods Clin. Dev., 2020, vol. 18, pp. 1−6. https://doi.org/10.1016/j.omtm.2020.05.013
Singanayagam, A., Hakki, S., Dunning, J., Madon, K.J., Crone, M.A., et al., Community transmission and viral load kinetics of the SARS-CoV-2 delta (B.1.617.2) variant in vaccinated and unvaccinated individuals in the UK: A prospective, longitudinal, cohort study, Lancet Infect. Dis., 2022, vol. 22, no. 2, pp. 183−195. https://doi.org/10.1016/S1473-3099(21)00648-4
Sun, Y., Lin, W., Dong, W., Xu, J., Origin and evolutionary analysis of the SARS-CoV-2 Omicron variant, J. Biosaf. Biosecur., 2022, vol. 4, no. 1, pp. 33−37. https://doi.org/10.1016/j.jobb.2021.12.001
Suzuki, R., Yamasoba, D., Kimura, I., Wang, L., Kishimoto, M., et al., Attenuated fusogenicity and pathogenicity of SARS-CoV-2 Omicron variant, Nature, 2022, vol. 603, no. 7902, pp. 700−705. https://doi.org/10.1038/s41586-022-04462-1
Swiss Policy Research, 2020. https://swprs.org/why-covid-19-is-a-strange-pandemic/.
Swiss Policy Research, 2021. https://swprs.org/covid-versus-the-flu-revisited/.
Thomine, O., Alizon, S., Boennec, C., Barthelemy, M., and Sofonea, M., Emerging dynamics from high-resolution spatial numerical epidemics, eLife, 2021, vol. 10, p. e71417. https://doi.org/10.7554/eLife.71417
VanBlargan, L.A., Errico, J.M., Halfmann, P.J., Zost, S.J., Crowe, J.E., Jr., et al., An infectious SARS-CoV-2 B.1.1.529 Omicron virus escapes neutralization by therapeutic monoclonal antibodies, Nat. Med., 2022, vol. 28, no. 3, pp. 490−495. https://doi.org/10.1038/s41591-021-01678-y
WHO, 2020. https://www.who.int/docs/default-source/ coronaviruse/who-china-joint-mission-on-covid-19-final-report.pdf.
Wong, J.P., Viswanathan, S., Wang, M., Sun, L.Q., Clark, G.C., and D’Elia, R.V., Current and future developments in the treatment of virus-induced hypercytokinemia, Future Med. Chem., 2017, vol. 9, no. 2, pp. 169–178. https://doi.org/10.4155/fmc-2016-0181
Yuan, M., Huang, D., Lee, C.D., Wu, N.C., Jackson, A.M., et al., Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants, Science, 2021, vol. 373, pp. 818−823. https://doi.org/10.1126/science.abh1139
Zhang, X., Wu, S., Wu, B., Yang, Q., Chen, A., et al., SARS-CoV-2 Omicron strain exhibits potent capabilities for immune evasion and viral entrance, Signal Transduction Targeted Ther., 2021, vol. 6, no. 1, p. 430. https://doi.org/10.1038/s41392-021-00852-5
Zurita-Gutiérrez, Y.H. and Lion, S., Spatial structure, host heterogeneity and parasite virulence: Implications for vaccine-driven evolution, Ecol. Lett., 2015, vol. 18, pp. 779–789. https://doi.org/10.1111/ele.12455
ACKNOWLEDGMENTS
The author thanks S.S. Zhukova for organizing a research seminar conducted by the author on the topic of this review, which formed the basis of this text. The author also expresses gratitude to M.E. Goltsman for his recommendation to write this review based on seminar materials and for a number of clarifications on the technical design of the manuscript, as well as for valuable comments on the section on modeling the evolution of viruses. Finally, the author thanks G.A. Bazykin, who read the full text of the manuscript, for valuable comments that helped improve the article.
Funding
This work was supported by ongoing institutional funding. No additional grants to carry out or direct this particular research were obtained.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
This work does not contain any studies involving human and animal subjects.
CONFLICT OF INTEREST
The author of this work declares that he has no conflicts of interest.
Additional information
Publisher’s Note.
Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Panchenko, P.L. Evolution of Viruses in Immunized Populations of Vertebrates. Biol Bull Rev 14, 43–59 (2024). https://doi.org/10.1134/S2079086424010079
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S2079086424010079