Phylodynamic theory of persistence, extinction and speciation of rapidly adapting pathogens

• DOI: 10.7554/elife.44205
• Publication Date: 2019-09-18T12:00:27Z
• Authors: Le Yan; Richard A Neher; Boris I Shraiman
• Keywords: 0301 basic medicine; Models, Genetic; extinction; QH301-705.5; Science; Q; Population Dynamics; R; Adaptation, Biological; Physics of Living Systems; Orthomyxoviridae; Antigenic Variation; Biological Evolution; 3. Good health; 03 medical and health sciences; speciation; Orthomyxoviridae Infections; evolution; host/pathogen; Medicine; Animals; Humans; Biology (General); Antigens, Viral

Rapidly evolving pathogens like influenza viruses can persist by changing their antigenic properties fast enough to evade the adaptive immunity, yet they rarely split into diverging lineages. By mapping the multi-strain Susceptible-Infected-Recovered model onto the traveling wave model of adapting populations, we demonstrate that persistence of a rapidly evolving, Red-Queen-like state of the pathogen population requires long-ranged cross-immunity and sufficiently large population sizes. This state is unstable and the population goes extinct or ‘speciates’ into two pathogen strains with antigenic divergence beyond the range of cross-inhibition. However, in a certain range of evolutionary parameters, a single cross-inhibiting population can exist for times long compared to the time to the most recent common ancestor (TM⁢R⁢C⁢A) and gives rise to phylogenetic patterns typical of influenza virus. We demonstrate that the rate of speciation is related to fluctuations ofTM⁢R⁢C⁢Aand construct a ‘phase diagram’ identifying different phylodynamic regimes as a function of evolutionary parameters.