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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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 |
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Open Polar |
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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 |
container_issue |
1 |
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1766345202610470912 |