Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms

Abstract Background Daily 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 p...

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Published in:Malaria Journal
Main Authors: Aidan J. O’Donnell, Sarah E. Reece
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2021
Subjects:
Online Access:https://doi.org/10.1186/s12936-021-03643-z
https://doaj.org/article/7be2818566e34aa9b2c37aa6b64f4aae
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spelling ftdoajarticles:oai:doaj.org/article:7be2818566e34aa9b2c37aa6b64f4aae 2023-05-15T15:14:47+02:00 Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms Aidan J. O’Donnell Sarah E. Reece 2021-02-01T00:00:00Z https://doi.org/10.1186/s12936-021-03643-z https://doaj.org/article/7be2818566e34aa9b2c37aa6b64f4aae EN eng BMC https://doi.org/10.1186/s12936-021-03643-z https://doaj.org/toc/1475-2875 doi:10.1186/s12936-021-03643-z 1475-2875 https://doaj.org/article/7be2818566e34aa9b2c37aa6b64f4aae Malaria Journal, Vol 20, Iss 1, Pp 1-12 (2021) Periodicity Synchrony Circadian rhythm Feeding timing Intraerythrocytic development cycle Asexual replication Arctic medicine. Tropical medicine RC955-962 Infectious and parasitic diseases RC109-216 article 2021 ftdoajarticles https://doi.org/10.1186/s12936-021-03643-z 2022-12-31T09:29:46Z Abstract Background Daily 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. Methods This 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. Results The 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. Conclusions Overall, 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. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic Malaria Journal 20 1
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Periodicity
Synchrony
Circadian rhythm
Feeding timing
Intraerythrocytic development cycle
Asexual replication
Arctic medicine. Tropical medicine
RC955-962
Infectious and parasitic diseases
RC109-216
spellingShingle Periodicity
Synchrony
Circadian rhythm
Feeding timing
Intraerythrocytic development cycle
Asexual replication
Arctic medicine. Tropical medicine
RC955-962
Infectious and parasitic diseases
RC109-216
Aidan J. O’Donnell
Sarah E. Reece
Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms
topic_facet Periodicity
Synchrony
Circadian rhythm
Feeding timing
Intraerythrocytic development cycle
Asexual replication
Arctic medicine. Tropical medicine
RC955-962
Infectious and parasitic diseases
RC109-216
description Abstract Background Daily 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. Methods This 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. Results The 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. Conclusions Overall, 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.
format Article in Journal/Newspaper
author Aidan J. O’Donnell
Sarah E. Reece
author_facet Aidan J. O’Donnell
Sarah E. Reece
author_sort Aidan J. O’Donnell
title Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms
title_short Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms
title_full Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms
title_fullStr Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms
title_full_unstemmed Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms
title_sort ecology of asynchronous asexual replication: the intraerythrocytic development cycle of plasmodium berghei is resistant to host rhythms
publisher BMC
publishDate 2021
url https://doi.org/10.1186/s12936-021-03643-z
https://doaj.org/article/7be2818566e34aa9b2c37aa6b64f4aae
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source Malaria Journal, Vol 20, Iss 1, Pp 1-12 (2021)
op_relation https://doi.org/10.1186/s12936-021-03643-z
https://doaj.org/toc/1475-2875
doi:10.1186/s12936-021-03643-z
1475-2875
https://doaj.org/article/7be2818566e34aa9b2c37aa6b64f4aae
op_doi https://doi.org/10.1186/s12936-021-03643-z
container_title Malaria Journal
container_volume 20
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