Evolutionary stability of the lysis‐lysogeny decision: why be virulent?

Abstract

Lytic viruses infect and kill host cells, producing a large number of viral copies. Temperate viruses, in contrast, are able to integrate viral genetic material into the host cell DNA, leaving a viable host cell. The evolutionary advantage of this strategy, lysogeny, has been demonstrated in complex environments that include spatial structure, oscillating population dynamics, or periodic environmental collapse. Here, we examine the evolutionary stability of the lysis–lysogeny decision, that is, we predict the long‐term outcome of the evolution of lysogeny rates. We demonstrate that viruses with high rates of lysogeny are stable against invasion by more virulent viral strains even in simple environments, as long as the pool of susceptible hosts is not unlimited. This mirrors well‐known results in both r‐K selection theory and virulence evolution: although virulent viruses have a faster potential growth rate, temperate strains are able to maintain positive growth on a lower density of the limiting resource, susceptible hosts. We then outline scenarios in which the rate of lysogeny is predicted to evolve either toward full lysogeny or full lysis. Finally, we demonstrate conditions under which intermediate rates of lysogeny, as observed in temperate viruses in nature, can be sustained long‐term. In general, intermediate lysogeny rates persist when the coupling between susceptible host density and virus density is relaxed.

When to be Temperate: On the Fitness Benefits of Lysis vs. Lysogeny

“…(4A) -red, purely lytic strategy is robust). This finding agrees with multiple recent studies of the evolution of viral strategies given long-term viral-host feedback (15,23,24). We also note that invasion by a mutant strain does not necessarily imply replacement of the resident strain.…”

“…For each temperate phage model, we construct the mutant-resident system, and compute the invasion fitness of mutant viral strains at the resident endemic equilibrium via a next-generation matrix approach (22,23); see SI Text, section 4.…”

Phage and bacteria diversification through a prophage acquisition ratchet

“…The accuracy of the model could be improved by adding the molecular mechanisms leading to the formation of new lysogens, which has been modeled at single strain-level but proven hard to incorporate into ecological scenarios (Steward and Levin 1984; Wang and Goldenfeld 2010; Maslov and Sneppen 2017; Wahl et al 2018; Weitz et al 2019; Chaudhry et al 2019). The accuracy could be also improved by incorporating by incorporating specific predator and immune system pressure (Thingstad and Lignell 1997; Thingstad 2000; Winter et al 2010; Dwayne et al 2017; Caron et al 2017; Talmy et al 2019), variable energy sources (Thingstad and Lignell 1997; Weitz et al 2015), and ecosystem-specific ranges for phage-bacteria traits and nested viral-microbial networks (Flores et al 2011; Thingstad et al 2014; Gao et al 2017; Hendricks 1972; Kirchman 2016; De Paepe and Taddei 2006).…”

How repeated outbreaks drive the evolution of bacteriophage communication: Insights from a mathematical model

“…In line with these model predictions, a combination of modelling and experimental work showed that selection pressures on phage virulence change over the course of an epidemic, favouring a virulent phage strain early on, when the density of susceptible cells is high, but a less virulent (i.e., lysogenic) phage strain later in the epidemic, when susceptible cells have become scarce [13,14]. Other modelling work has shown that if phages, lysogenised cells, and susceptible cells coexist for long periods of time, the susceptible cell density becomes low because of phage exploitation, and less and less virulent phages are selected [15,16].Erez et al [9] propose that the arbitrium system may have evolved to allow phages to cope with the changing environment during an epidemic, allowing the phages to exploit available susceptible bacteria through the lytic cycle when few infections have so far taken place and hence the concentration of arbitrium is low, while entering the lysogenic cycle when many infections have taken place and the arbitrium concentration has hence increased. This explanation resembles results for other forms of phage-phage interaction previously found in Escherichia coli -infecting phages [17,18].…”

“…Free phage particles decay at a rate δ and adsorb to bacteria at a rate a. Adsorptions to lysogens result in the decay of the infecting phage, thus describing the well-known effect of superinfection immunity [25][26][27][28][29], while adsorptions to susceptible bacteria result in infections with success probability b. We consider the lytic cycle to be fast compared to both bacterial growth and the lysogenic cycle (c.f., [11,13,16,24]), so that a lytic infection can be modelled as immediate lysis releasing a burst of B free phages. Since the genes encoding arbitrium production are among the first genes to be expressed when a phage…”