Abstract
BackgroundDaily periodicity in the diverse activities of parasites occurs across a broad taxonomic range. The rhythms exhibited by parasites are thought to be adaptations that allow parasites to cope with, or exploit, the consequences of host activities that follow daily rhythms. Malaria parasites (Plasmodium) are well-known for their synchronized cycles of replication within host red blood cells. Whilst most species of Plasmodium appear sensitive to the timing of the daily rhythms of hosts, and even vectors, some species present no detectable rhythms in blood-stage replication. Why the intraerythrocytic development cycle (IDC) of, for example Plasmodium chabaudi, is governed by host rhythms, yet seems completely independent of host rhythms in Plasmodium berghei, another rodent malaria species, is mysterious.MethodsThis study reports a series of five experiments probing the relationships between the asynchronous IDC schedule of P. berghei and the rhythms of hosts and vectors by manipulating host time-of-day, photoperiod and feeding rhythms.ResultsThe results reveal that: (i) a lack coordination between host and parasite rhythms does not impose appreciable fitness costs on P. berghei; (ii) the IDC schedule of P. berghei is impervious to host rhythms, including altered photoperiod and host-feeding-related rhythms; (iii) there is weak evidence for daily rhythms in the density and activities of transmission stages; but (iv), these rhythms have little consequence for successful transmission to mosquitoes.ConclusionsOverall, host rhythms do not affect the performance of P. berghei and its asynchronous IDC is resistant to the scheduling forces that underpin synchronous replication in closely related parasites. This suggests that natural variation in the IDC schedule across species represents different parasite strategies that maximize fitness. Thus, subtle differences in the ecological interactions between parasites and their hosts/vectors may select for the evolution of very different IDC schedules.
Highlights
Periodicity in the diverse activities of parasites occurs across a broad taxonomic range
Hosts, and vectors Hosts were either wild type (WT) MF1 mice or Per1/2-null clock-disrupted mice previously backcrossed onto a C57BL/6J background for over 10 generations, all sourced from inhouse breeding colonies
Experiment 2: does the intraerythrocytic development cycle (IDC) become synchronous in long days? Experiment 2 tested Arnold’s [34] observation that the IDC of P. berghei becomes synchronous in long days
Summary
Periodicity in the diverse activities of parasites occurs across a broad taxonomic range. The rhythms exhibited by parasites are thought to be adaptations that allow parasites to cope with, or exploit, the consequences of host activities that follow daily rhythms. Malaria parasites (Plasmodium) are well-known for their synchronized cycles of replication within host red blood cells. Whilst most species of Plasmodium appear sensitive to the timing of the daily rhythms of hosts, and even vectors, some species present no detectable rhythms in blood-stage replication. Other rhythmic activities are thought to enable parasites to cope with challenges imposed by, and exploit opportunities provided by, rhythms in the within-host environment. Botrytis cinerea, a fungal pathogen of Arabidopsis thaliana, has canonical clock (transcription–translation-feedback-loop) controlled rhythms in virulence that enable it to overwhelm hosts defenses when they are upregulated in the evening [5, 6]. Trypanosoma brucei uses a clock of unknown components to control gene expression of over two hundred of its genes, potentially allowing it to coordinate its metabolism with that of the host [7]
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