Host phenology can select for multiple stable parasite virulence strategies

Host phenology is an important driver of parasite transmission and evolution. In a seasonal environment, monocyclic, obligate-killer parasites evolve optimal virulence strategies such that all parasite progeny are released near the end of the host season to limit parasite progeny death in the environment. It is unclear whether host seasonality imposes different constraints on polycyclic parasites such that both polycyclic and monocyclic parasites are maintained. We develop a mathematical model of a disease system with seasonal host activity to study the evolutionary consequences of host phenology on polycyclic, obligate-killer parasite virulence strategies. Seasonal host activity patterns create both monocyclic and polycyclic parasite evolutionarily stable strategies (ESS) separated by less-fit strategies (evolutionary repellors). The ESS that evolves in each system is a function of the virulence strategy of the parasite introduced into the system. The trait value for both monocyclic and polycyclic strategies is determined by two aspects of host phenology: the duration of the host activity period and the distribution in the time at which hosts first become active within each season. Longer host activity periods and more synchronous host emergence drive both the monocyclic and polycyclic strategies towards lower virulence. The results demonstrate that host phenology can, in theory, maintain diverse parasite strategies among isolated geographic locations.

How host phenology impacts multi-season epidemic cycles

Parasite-host interactions can result in periodic population dynamics when parasites over-exploit host populations. The timing of host seasonal activity, or host phenology, determines the frequency and demographic impact of parasite-host interactions which may govern if the parasite can sufficiently over-exploit their hosts to drive population cycles. We describe a mathematical model of a monocyclic, obligate-killer parasite system with seasonal host activity to investigate the consequences of host phenology on host-parasite dynamics. The results suggest that parasites can reach the densities necessary to destabilize host dynamics and drive cycling in only some phenological scenarios, such as environments with short seasons and synchronous host emergence. Further, only parasite lineages that are sufficiently adapted to phenological scenarios with short seasons and synchronous host emergence can achieve the densities necessary to over-exploit hosts and produce population cycles. Host-parasite cycles can also generate an eco-evolutionary feedback that slows parasite adaptation to the phenological environment as rare advantageous phenotypes are driven to extinction when introduced in phases of the cycle where host populations are small and parasite populations are large. The results demonstrate that seasonal environments can drive population cycling in a restricted set of phenological patterns and provides further evidence that the rate of adaptive evolution depends on underlying ecological dynamics.

Host phenology drives the evolution of intermediate parasite virulence

1AbstractMechanistic trade-offs between transmission and virulence are the foundation of current theory on the evolution of parasite virulence. Empirical evidence supporting these trade-offs in natural systems remains elusive, suggesting other factors could drive virulence evolution in the absence of a mechanistic trade-off. Several ecological factors modulate the optimal virulence strategies predicted from mechanistic trade-off models but none have been sufficient to explain the intermediate virulence strategies observed in most natural systems. The timing of seasonal activities, or phenology, is a common factor that influences the types and impact of many ecological interactions but is rarely considered in virulence evolution studies. We develop a mathematical model of a disease system with seasonal host activity to study the evolutionary consequences of host phenology on parasite virulence. Seasonal host activity is sufficient to drive the evolution of intermediate parasite virulence in the absence of traditional mechanistic trade-offs. The optimal virulence strategy is determined by both the duration of the host activity period as well as the variation in the host emergence timing. Parasites with low virulence strategies are favored in environments with long host activity periods and in environments in which all hosts emerge synchronously. These results demonstrate that host phenology may be sufficient, in the absence of mechanistic trade-offs, to select for intermediate optimal virulence strategies in some natural systems.

The role of host phenology for parasite transmission

Phenology is a fundamental determinant of species distributions, abundances, and interactions. In host–parasite interactions, host phenology can affect parasite fitness due to the temporal constraints it imposes on host contact rates. However, it remains unclear how parasite transmission is shaped by the wide range of phenological patterns observed in nature. We develop a mathematical model of the Lyme disease system to study the consequences of differential tick developmental-stage phenology for the transmission of B. burgdorferi. Incorporating seasonal tick activity can increase B. burgdorferi fitness compared to continuous tick activity but can also prevent transmission completely. B. burgdorferi fitness is greatest when the activity period of the infectious nymphal stage slightly precedes the larval activity period. Surprisingly, B. burgdorferi is eradicated if the larval activity period begins long after the end of nymphal activity due to a feedback with mouse population dynamics. These results highlight the importance of phenology, a common driver of species interactions, for the fitness of a parasite.

The role of host phenology for parasite transmission

Phenology is a fundamental determinant of species distributions, abundances, and interactions. In host-parasite interactions, host phenology can affect parasite fitness due to the temporal constraints it imposes on host contact rates. However, it remains unclear how parasite transmission is shaped by the wide range of phenological patterns observed in nature. We develop a mathematical model of the Lyme disease system to study the consequences of differential tick developmental-stage phenology for the transmission of B. burgdorferi. Incorporating seasonal tick activity can increase B. burgdorferi fitness compared to continuous tick activity but can also prevent transmission completely. B. burgdorferi fitness is greatest when the activity period of the infectious nymphal stage slightly precedes the larval activity period. Surprisingly, B. burgdorferi is eradicated if the larval activity period begins long after the end of nymphal activity due to a feedback with mouse population dynamics. These results highlight the importance of phenology, a common driver of species interactions, for the fitness of a parasite.