Abstract
The prevailing paradigm in eco-evolutionary studies of viruses and their microbial hosts is that the reproductive success of viruses depends on the proliferation of the “predator”, i.e., the virus particle. Yet, viruses are obligate intracellular parasites, and the virus genome – the actual unit of selection – can persist and proliferate from one cell generation to the next without lysis and the production of new virus particles. Here, we propose a unified theory of virus-microbe dynamics that addresses the inherent tension between horizontal and vertical modes of viral reproduction. In doing so we propose a cell-centric metric for quantifying the ‘fitness’ of viruses that infect microorganisms. This cell-centric metric takes an epidemiological perspective that enables direct comparison of viral strategies characterized by obligate killing of hosts (e.g., via lysis), persistence of viral genomes inside hosts (e.g., via lysogeny), and strategies along a continuum between these extremes (e.g., via chronic infections). As a result, we can identify those environmental drivers, life history traits, and key feedbacks that govern variation in viral propagation in nonlinear population models. For example, we identify threshold conditions given relatively low cell densities and relatively high cell growth rates in which lysogenic and other persistent strategies have higher potential viral reproduction than lytic strategies. By focusing on the proliferation of viral genomes inside cells instead of virus particles outside cells, the present theory unifies the study of eco-evolutionary drivers of viral strategies in natural environments.