The Life and Times of Parasites: Rhythms in Strategies for Within-host Survival and Between-host Transmission

Abstract

Biological rhythms are thought to have evolved to enable organisms to organize their activities according to the earth's predictable cycles, but quantifying the fitness advantages of rhythms is challenging and data revealing their costs and benefits are scarce. More difficult still is explaining why parasites that live exclusively within the bodies of other organisms have biological rhythms. Rhythms exist in the development and traits of parasites, in host immune responses, and in disease susceptibility. This raises the possibility that timing matters for how hosts and parasites interact and, consequently, for the severity and transmission of diseases. Here, we take an evolutionary ecological perspective to examine why parasites exhibit biological rhythms and how their rhythms are regulated. Specifically, we examine the adaptive significance (evolutionary costs and benefits) of rhythms for parasites and explore to what extent interactions between hosts and parasites can drive rhythms in infections. That parasites with altered rhythms can evade the effects of control interventions underscores the urgent need to understand how and why parasites exhibit biological rhythms. Thus, we contend that examining the roles of biological rhythms in disease offers innovative approaches to improve health and opens up a new arena for studying host-parasite (and host-parasite-vector) coevolution.

Keywords: Plasmodium; adaptation; chronobiology; circadian rhythm; fitness; host-parasite interactions; life history; phenotypic plasticity; transmission.

Figure 1.

Selection of the rhythmic factors (cogs) in the various environments that parasites experience during their lifecycles that are hypothesized to shape rhythms in parasite traits. Rhythmic factors within each environment are often correlated and can shape the rhythms of factors in other environments (dotted arrows). The complexity of the possible combinatorial interactions between rhythmic environmental factors and the diversity of parasite rhythms that can be affected poses an interdisciplinary challenge in regard to unravelling what drives parasite rhythms and their consequences for fitness.

Figure 2.

The migration of microfilariae from the lungs to the host’s peripheral circulation broadly coincides with the activity rhythms of their mosquito vector species. Red lines illustrate rhythms in the percentage of the maximum number of microfilariae observed in the peripheral blood of hosts, and the bars illustrate vector biting activity. (A) The nocturnally periodic form of Wuchereria bancrofti is transmitted by night-biting Anopheles and Culex, and (B) the diurnally subperiodic form is transmitted by day-biting Aedes. Coinciding migration with vector foraging is thought to maximize parasite transmission, the “Hawking hypothesis.” Adapted from Pichon and Treuil (2004).