Publications

For pdfs of our publications, please click the paper titles.

 

2024

Oke, C. E., O'Donnell, A. J., Schneider, P., & Reece, S. E. (2024). Plasticity in malaria parasite development: mosquito resources influence vector-to-host transmission potential. Frontiers in Malaria, 2, 1481816. https://doi.org/10.3389/fmala.2024.1481816

Parasites rely on their hosts for all their nutrition however mosquitoes in the field exhibit diversity in the amount of food they require. In this paper we ask how variation in the amount of sugar and blood provided to malaria-infected mosquitoes affects the potential for parasites to transmit from vector to host. We find that parasites in well resourced mosquitoes are bigger, faster and are more numerous. Our results also suggest that resource availability affects the ability of parasites to migrate from the midgut to salivary glands for transmission.

Holland, J. G., Prior, K. F., O’Donnell, A. J., & Reece, S. E. (2024). Testing the evolutionary drivers of malaria parasite rhythms and their consequences for host–parasite interactions. Evolutionary Applications, 17, e13752. https://doi.org/10.1111/eva.13752

We perturb several rhythms in the hosts of malaria parasites to investigate why parasites align their rhythmic replication to the host's feeding-fasting rhythm. We manipulated host rhythms governed by light, food or both, and assessed the fitness implications for par- asites to test which host rhythms represent ultimate drivers of the parasite's rhythm. We found that the host's light-driven rhythms did not affect parasite fitness but aligning with the timing of feeding-fasting rhythms may be beneficial for the parasite when the host possess a functional canonical circadian clock. Our results also suggest cue(s) from host food act as a proxy rather than being a key selective driver of the parasite's rhythm.

Greischar, M. A., Savill, N. J., Reece, S. E., & Mideo, N. (2024). How to quantify developmental synchrony in malaria parasites. bioRxiv, 2024-02. https://doi.org/10.3389/fmala.2024.1386266

Malaria infections represent an iconic example of developmental synchrony, where periodic fevers can result when the population of parasites develops synchronously within host red blood cells. Synchrony appears to vary across individual hosts and across parasite species and strains, but current approaches for quantifying synchrony in parasites are often biased, so we develop an approach to estimate synchrony that accounts for population dynamics.

Owolabi, A. T. Y., Schneider, P., and Reece, S. E. (2024). Virulence is associated with daily rhythms in the within-host replication of the malaria parasite Plasmodium chabaudi. Evolutionary Applications (17): e13696. https://doi.org/10.1111/eva.1396

This paper investigates the link between virulence and parasite synchrony and finds evidence for the hypothesis that virulence is negatively correlated with synchrony (i.e. the more synchronous a population of parasites the less virulent the infection).

Westwood, M. L., Geissmann, Q., O’Donnell, A. J., Rayner, J., Schneider, W., Zuk, M., Bailey, N. W. and Reece, S. E. (2024). Machine learning reveals singing rhythms of male Pacific field crickets are clock controlled. Behavioral Ecology, 35(1), p.arad098. https://doi.org/10.1093/beheco/arad098

Evidence from field work suggests that male Pacific field crickets are changing the time of day they sing potentially as an anti-parasitoid strategy. We demonstrate that male calling behaviour meets all criteria for being an endogenous trait controlled by the circadian clock and thus could be a target for natural selection imposed by the parasitoid.

2023

Oke, C. E., Reece, S. E., & Schneider, P. (2023). Testing a non-destructive assay to track Plasmodium sporozoites in mosquitoes over time. Parasites & Vectors, 16(1), 1-12. https://doi.org/10.1186/s13071-023-06015-5

We tested a non-destructive method to detect sporozoites from individual infected mosquitoes on sugar-feeding substrates. Detection rate was surprisingly low, and investigations of the biological causes underlying this is needed to maximise the utility of using non-destructive assays to quantify sporozoite dynamics

Mainero, A. H., Spence, P. J., Reece, S. E., & Kamiya, T. (2023). The impact of innate immunity on malaria parasite infection dynamics in rodent models. Frontiers in Immunology, 14. https://doi.org/10.3389/fimmu.2023.1171176

We conduct a meta-analysis to seek consensus on the effect of innate immunity on parasite replication, examining three different species of rodent malaria parasite. The small effect sizes we observe following experimental perturbations of the innate immune system may be explained by redundancy in a complex biological system or by incomplete (or inappropriate) data reporting for meta-analysis. Alternatively, our findings suggest the need to re-evaluate the efficiency with which innate immunity controls parasite replication early in infection.

2022

Labeed, F. H., Beale, A. D., Schneider, P., Kitcatt, S. J., Kruchek, E. J., & Reece, S. E. (2022) Circadian rhythmicity in murine blood: Electrical effects of malaria infection and anemia. Frontiers in Bioengineering and Biotechnology, 10. https://doi.org/10.3389/fbioe.2022.994487

Red blood cells have circadian rhythms in electrophysiological properties that are affected differently by anaemia and by malaria infection.

Kamiya, T., Paton, D. G., Catteruccia, F., & Reece, S. E. (2022). Targeting malaria parasites inside mosquitoes: ecoevolutionary consequences. Trends in Parasitology. https://doi.org/10.1016/j.pt.2022.09.004

Illustrates the broader evolutionary guidance we provide, by revealing that using antimalarials to kill Plasmodium inside mosquitoes has potential to be more robust to resistance evolution than current approaches, and could extend the lifespan and clinical benefit of antimalarials used exclusively to treat humans.

Oke C. E., Ingham, V. A., Walling C. A., Reece, S. E. (2022) Vector control: agents of selection on malaria parasites? Trends in Parasitology 2022. https://doi.org/10.1016/j.pt.2022.07.006.

This review highlights how vector control tools such as insecticides have altered mosquito vectors and consequently parasite ecology, and discusses how parasites might be able to respond. Understanding parasite responses is important because they could undermine gains made towards malaria elimination and may have knock-on consequences for parasite-host interactions.

2021

O’Donnell A. J., Greischar M. A., & Reece, S. E. (2021) Mistimed malaria parasites re‐synchronise with host feeding‐fasting rhythms by shortening the duration of intra‐erythrocytic development. Parasite Immunology, e12898. https://doi.org/10.1111/pim.12898

Here we demonstrate that parasites that are out of synchrony with host feeding rhythms can reschedule themselves by shortening the duration of their development cycle.

Prior K. F., Middleton B., Owolabi A. T. Y., Westwood M. L., Holland, J., O'Donnell A. J., Blackman M. J., Skene D. J., Reece S. E. (2021) Synchrony between daily rhythms of malaria parasites and hosts is driven by an essential amino acid. Wellcome Open Res 2021, 6:186 https://doi.org/10.12688/wellcomeopenres.16894.2

Screens for rhythmic metabolites in the blood of infected mice whose timing matches that of both host feeding/fasting and the IDC schedule (across perturbations of host and parasite rhythms). Finds a single candidate, isoleucine, and in vitro tests reveal isoleucine fulfils all criteria of a time-cue.

Owolabi, A. T., Reece, S. E., & Schneider, P. (2021). Daily rhythms of both host and parasite affect antimalarial drug efficacy. Evolution, Medicine, and Public Health. https://doi.org/10.1093/emph/eoab013

Demonstrates how chronotherapy (providing medicines at a particular time-of-day) can improve treatment for malaria infections. Specifically, parasites’ developmental stage at the time of treatment and the coordination of timing between parasite and host both affect how well antimalarial drug treatment works

Schneider P., Reece, S. E. (2021) The private life of malaria parasites: strategies for sexual reproduction. Molecular & Biochemical Parasitology. https://doi.org/10.1016/j.molbiopara.2021.111375

We outline how evolutionary and ecological theories, developed to explain reproductive strategies in multicellular taxa, can be applied to explain two reproductive strategies (conversion rate and sex ratio) expressed by malaria parasites within the vertebrate host.

O’Donnell, A. J., Reece, S. E. (2021) Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms.Malaria Journal 20, 105. https://doi.org/10.1186/s12936-021-03643-z

Demonstrates that the various peturbations that normally lead to synchronisation of parasite cycles in P. chabaudi do not have the same effect on a related species, P. berghei.

Davidson, M. S., Yahiya, S., Chmielewski, J., O’Donnell, A. J., Gurung, P., Jeninga, M., Prommana, P., Andrew, D., Petter, M, Uthaipibull, C., Boyle, M., Ashdown, G. W., Dvorin, J. D., Reece, S. E., Wilson, D. W., Ando, D. M., Dimon, M. & Baum, J. (2021). Automated detection and staging of malaria parasites from cytological smears using convolutional neural networks. medRxiv. https://doi.org/10.1101/2021.01.26.21250284

Describes a novel machine learning method for identifying and staging parasites from microscopy images.

2020

Subudhi A. K., O’Donnell A. J., Ramaprasad A., Abkallo H. M., Kaushik A., Ansari H. R., Abdel-Haleem A. M., Rached F. B., Kaneko O., Culleton R., Reece S. E. & Pain, A. (2020). Malaria parasites regulate intra-erythrocytic development duration via serpentine receptor 10 to coordinate with host rhythms. Nature Communications 11(2763). https://doi.org/10.1038/s41467-020-16593-y

Demonstrates that: 57% of P. chabaudi’s and 6% of P. falciparum’s genes are expressed with 24hr rhythms; rhythmicity is lost in half of P. chabaudi’s genes when misaligned to host rhythms; and SR10 determines the IDC duration. Provides insight into why misalignment reduces fitness and reveals parasite control of the IDC schedule.

Prior K. F., Rijo-Ferreira F., Assis P. A., Hirako I. C., Weaver D. R., Gazzinelli R. T., Reece S. E. (2020). Periodic Parasites and Daily Host Rhythms. Cell Host Microbe, 27(2):6-187. doi:https://doi.org/10.1016/j.chom.2020.01.005

Invited. Develops testable hypotheses for how rhythmicity in Plasmodium replication and transmission traits is generated, why these rhythms matter for parasite fitness, and how this knowledge can be harnessed for interventions.

Westwood M. L., O’Donnell A. J., Schneider P., Albery G. F., Prior K. F., & Reece S. E. (2020). Testing possible causes of gametocyte reduction in temporally out-of-synch malaria infections. Malaria Journal, 19(1):1-10. https://doi.org/10.1186/s12936-020-3107-1

Tests whether the observed 50% reduction in gametocytes in temporally mismatched parasites can be explained by a reduction in conversion rate or increased cleareance by the hosts immune responses

O'Donnell A. J., Prior K. F. and Reece S. E. (2020). Host circadian clocks do not set the schedule for the within-host replication of malaria parasites. Proceedings of the Royal Society B 287: 20200347. http://dx.doi.org/10.1098/rspb.2020.0347

Pairs with Prior et al 2018: Reveals that synchrony and timing of the IDC follows rhythms associated with host feeding/fasting that are independent of the host’s canonical circadian clock (including the light-entrained oscillator in the brain and the transcription-translation-feedback-loop within all cells). Further, IDC synchrony dampens in the absence of feeding/fasting rhythms. Subsequently verified by others.

2019

Birget P. L. G., Schneider P., O’Donnell A. J., & Reece S. E. (2019). Adaptive phenotypic plasticity in malaria parasites is not constrained by previous responses to environmental change. Evolution, Medicine, and Public Health, eoz028. https://doi.org/10.1093/emph/eoz028

Malaria parasites have evolved flexible strategies to cope with the changing conditions they experience during infections. We show that using such flexible strategies does not impact upon the parasites’ ability to grow (resulting in disease symptoms) or transmit (spreading the disease).

Prior K. F., O’Donnell A. J., Rund S. S., Savill N. J., van der Veen D. R., & Reece S. E. (2019). Host circadian rhythms are disrupted during malaria infection in parasite genotype-specific manners. Scientific Reports, 9:10905. https://doi.org/10.1038/s41598-019-47191-8

Characterises differences infection dynamics in three parasite genotypes in response to timing disruption and shows that the disruption is a genetically variable virulence trait

Birget P. L., Prior K. F., Savill N. J., Steer, L. & Reece S. E. (2019). Plasticity and genetic variation in traits underpinning asexual replication of the rodent malaria parasite, Plasmodium chabaudi. Malaria journal, 18(1):222. https://doi.org/10.1186/s12936-019-2857-0

Demonstrates previously unknown plasticity and genetic variation in parasite traits such as cell cycle duration, burst size and RBC preference in response to host anaemia

O’Donnell A. J., Rund S. S. C., Reece S. E. (2019). Time-of-day of blood-feeding: effects on mosquito life history and malaria transmission. Parasites & vectors, 12(1):301. https://doi.org/10.1186/s13071-019-3513-9

With reports of mosquitoes biting earlier in the day as a strategy to avoid insecticide treated bed nets, this paper explores the consequence of altered biting time on mosquito life history and parasite trasmission

Schneider P., Babiker H. A., Gadalla A. A. H, Reece S. E. (2019). Evolutionary sex allocation theory explains sex ratios in natural Plasmodium falciparum infections. International Journal for Parasitology, [Accepted 5/4/19] https://doi.org/10.1016/j.ijpara.2019.04.001.

Applies evolutionary sex allocation theroy to human malaria infections to demonstrate that parasites have a form of 'fertility insurance' in which gametocyte sex ratios are negatively correlated with density.

Greischar M. A.,Reece S. E., Savill N. J., & Mideo N. (2019). The Challenge of Quantifying Synchrony in Malaria Parasites. Trends in Parasitology, 35(5). https://doi.org/10.1016/j.pt.2019.03.002

Comparing the degree of synchrony across species, strains, and time points within infection can illuminate the proximate and evolutionary drivers of synchrony. Standardized methods for comparing synchrony are lacking and may suffer from multiple sources of bias, highlighting an urgent need for better approaches

Westwood M. L., O’Donnell A. J., de Bekker C., Lively C. M., Zuk M., & Reece, S. E. (2019). The evolutionary ecology of circadian rhythms in infection.Nature ecology & evolution, 18(1). https://doi.org/10.1038/s41559-019-0831-4

Explores how hosts use rhythms to defend against infection, why parasites have rhythms and whether parasites can manipulate host clocks to their own ends.

2018

Lippens C., Guivier E., Reece S. E., O’Donnell A. J., Cornet S., Faivre B., & Sorci G. (2018). Early Plasmodium‐induced inflammation does not accelerate aging in mice. Evolutionary Applications, 12(2):314-23.https://doi.org/10.1111/eva.12718

Tests the hypothesis that early activation of the inflammatory response confers protection against infection, it results in reduced reproductive output at old age and shortened longevity.

Schneider P., Greischar M. A., Birget P. L. G., Repton C., Mideo N., & Reece, S. E. (2018). Adaptive plasticity in the gametocyte conversion rate of malaria parasites PLoS Pathogens, 14(11):e1007371. https://doi.org/10.1371/journal.ppat.1007371

Demonstrates Plasmodium alters transmission investment, according how a range of stressors change within-host population size. When population sizes plummet, parasites prioritise between-host transmission but smaller losses in number elicit reproductive restraint, which facilitates in-host survival and future transmission. Unites previously contradictory observations about ‘conversion rate’ variation across the genus.

Schneider P., Rund S. S. C., Smith N. L., Prior K. F., O'Donnell A. J., & Reece S. E. (2018). Adaptive periodicity in the infectivity of malaria gametocytes to mosquitoes. Proceedings of the Royal Society B, 285(1888):20181876. https://doi.org/10.1098/rspb.2018.1876

Reveals gametocytes are twice as infective at night to mosquitoes and that vector rhythms also affect transmission. Answers a longstanding question posed by Hawking in the 1960’s but plagued with poor study design until now. Subsequently verified by others

Reece S. E., & Schneider P. (2018). Premature Rejection of Plasticity in Conversion. Trends in parasitology, 34(8):633. https://doi.org/10.1016/j.pt.2018.06.004

Comment on Koepfli et al (2018) to highlight the potential for parasites in natural infections of humans to adjust their investment in gametocytes during infections.

Reece S.E. and Prior K.F. (2018) Malaria Makes the Most of Mealtimes. Cell Host & Microbe, 23(6):695-7. https://doi.org/10.1016/j.chom.2018.05.015

News & Views article on Hirako, I.C., Assis, P.A., Hojo-Souza, N.S., Reed, G., Nakaya, H., Golenbock, D.T., Coimbra, R.S., and Gazzinelli, R.T. (2018). Daily rhythms of TNFa expression and food intake regulate synchrony of Plasmodium stages with host circadian cycle. Cell Host Microbe 23, this issue, 796–808.

Prior K. F., van der Veen D. R., O'Donnell A. J., Cumnock K., Schneider D., Pain A., Subudhi A., Ramaprasad A., Rund S. S. C., Savill N. J., & Reece S. E. (2018) Timing of host feeding drives rhythms in parasite replication. PLOS Pathogens, 14(2):e1006900. https://doi.org/10.1371/journal.ppat.1006900

and

O'Donnell A. J., Prior K. F. and Reece S. E. (2020). Host circadian clocks do not set the schedule for the within-host replication of malaria parasites. Proceedings of the Royal Society B 287: 20200347. http://dx.doi.org/10.1098/rspb.2020.0347

Reveals that synchrony and timing of the IDC follows rhythms associated with host feeding/fasting that are independent of the host’s canonical circadian clock (including the light-entrained oscillator in the brain and the transcription-translation-feedback-loop within all cells). Further, IDC synchrony dampens in the absence of feeding/fasting rhythms. Subsequently verified by others.

2017

Reece S. E., Prior K. F., & Mideo N. (2017) The Life and Times of Parasites: Rhythms in Strategies for Within-host Survival and Between-host Transmission Journal of Biological Rhythms, 32(6):516-33. https://doi.org/10.1177%2F0748730417718904

Examines why parasites exhibit biological rhythms and how their rhythms are regulated. Specifically, the adaptive significance (evolutionary costs and benefits) of rhythms for parasites and to what extent interactions between hosts and parasites can drive rhythms in infections

Birget P. L., Repton C., O'Donnell A. J., Schneider P., & Reece S. E. (2017) Phenotypic plasticity in reproductive effort: malaria parasites respond to resource availability Proceedings of the Royal Society B, 284(1860):20171229. https://doi.org/10.1098/rspb.2017.1229

Reveals that the malaria parasite Plasmodium chabaudi responds to host anaemia by increasing investment in transmission stages because, counterintuitively, host aneamia represents a better environment for parasite replication. Furthermore, evolutionary potential in form of genetic variation exists in the extent that parasite strains respond to changes in red blood cell resources.

Birget P. L.G., Greischar M., Reece S. E. & Mideo N. (2017) Altered life-history strategies protect malaria parasites against drugs Evolutionary applications, 11(4):442-55. https://doi.org/10.1111/eva.12516

Uses a within-host model of malaria infection to show that over a range of drug doses, parasites are predicted to adopt “reproductive restraint” (investing more in asexual replication and less in transmission to partially compensate for the fitness loss due to drugs.

2016

Ramiro R. S., Pollitt L. C., Mideo N. & Reece S. E. (2016) Facilitation through altered resource availability in a mixed-species rodent malaria infection Ecology Letters, 19(9):1041-50. https://doi.org/10.1111/ele.12639

Outlines how resource limitations can shape how parasite species interact within a co-infection and the epidemiological consequences of these interactions

Rund S. S. C., O’Donnell A. J., Gentile J. E. & Reece, S. E. (2016) Daily Rhythms in Mosquitoes and Their Consequences for Malaria Transmission. Insects, 7(2):14. https://doi.org/10.3390/insects7020014

Outlines new hypotheses for how daily rhythms in mosquitoes affects their capacity to transmit malaria parasites.

Carter L. M., Pollitt L. C., Wilson L. G. & Reece S. E. (2016) Ecological influences on the behaviour and fertility of malaria parasites. Malaria Journal, 15(1):220. https://doi.org/10.1186/s12936-016-1271-0

Examines how aspects of the physical and chemical environment experienced in the mosquito blood meal affects the ability of parasites to mate and suggest that male gametes are attracted to females by chemotaxis.

Greischar M. A, Reece S. E. & Mideo N. (2016) The role of models in translating within-host dynamics to parasite evolution. Parasitology, 143(7):905-14. https://doi.org/10.1017/S0031182015000815

Discusses how and why mathematical models are important for understanding the impact of infection processes for parasite evolution.

2015

Schneider P., Reece S. E.♯, van Schaijk B., Bousema T., Lanke K. H. W., Meaden C. S. J., Gadalla A., Ranford-Cartwright L. C. & Babiker H.♯ (2015) Quantification of male and female Plasmodium falciparum gametocytes by reverse-transcriptase quantitative PCR. Molecular and Biochemical Parasitology, 199(1-2):29-33. https://doi.org/10.1016/j.molbiopara.2015.03.006 ♯equal contributions

Presents new assays to separately count the number of male and female gametocytes of the human malaria parasite, P. falciparum.

Ramiro R. S., Khan S. M., Franke-Fayed B., Janse C. J., Obbard D. J., & Reece S. E. (2015) Hybridisation and pre-zygotic reproductive barriers in Plasmodium. Proceedings of the Royal Society B, 282(1806):20143027. https://doi.org/10.1098/rspb.2014.3027

Demonstrates that low levels of hybridization between different parasite species can occur and identifies some of the molecules involved in preventing this in nature.

2014

Reece S. E. & Mideo N. (2014). Malaria parasites prepare for flight. Trends in Parasitology, 30(12):551-3. https://doi.org/10.1016/j.pt.2014.10.004

Highlights a paper demonstrating that malaria parasites detect when mosquitoes bite their host and respond by investing in transmission.

Carter L. M., Schneider P. & Reece S. E. (2014) Information use and plasticity in the reproductive decisions of malaria parasites. Malaria Journal, 13(1):115. https://doi.org/10.1186/1475-2875-13-115

Narrows down the search for the information that malaria parasites use during infections to make decisions about investing in gametocytes (sexual stages) and their sex ratio.

Leggett H. C., Brown S. P. & Reece S. E. (2014). War and peace: social interactions in infections. Philosophical Transactions of the Royal Society B, 369(1642):20130365. https://doi.org/10.1098/rstb.2013.0365

Review of how parasites and microbial pathogens interact during infections and the implications for the severity and transmission of disease.

2013

O’Donnell A. J., Mideo N. & Reece S. E. (2013) Disrupting rhythms in Plasmodium chabaudi: costs accrue quickly and independently of how infections are initiated. Malaria Journal, 12(1):372. https://doi.org/10.1186/1475-2875-12-372

Asks whether parasites matched to the host's circadian rhythm are better able to establish infections than mismatched parasites

A correction has been published for this article: O’Donnell A.J., Mideo N. and > Reece S.E.> (2014) > Correction: Disrupting rhythms in > Plasmodium chabaudi> : costs accrue quickly and independently of how infections are initiated.> Malaria Journal, 13(1):503. > https://doi.org/10.1186/1475-2875-13-503

Fuller W. J., Godley B. J., Hodgson D.J., Reece S. E., Witt M. J. & Broderick A. C. (2013) The importance of spatio-temporal data for predicting the effects of climate change on marine turtle sex ratios. Marine Ecology Progress Series, 488:267-74. https://doi.org/10.3354/meps10419

Assesses the impact of climate change on species with temperature-dependent sex determination and the need for accurate data to predict these effects.

Viney M. & Reece S. E. (2013) Adaptive noise. Proceedings of the Royal Society B, 280(1767):20131104. https://doi.org/10.1098/rspb.2013.1104

Review: Sources for, and adaptation of, noise in gene expression.

Wilson L. G., Carter L. M. & Reece S. E. (2013) High-speed holographic microscopy of malaria parasites reveals ambidextrous flagellar waveforms. Proceedings of the National Academy of Sciences, 110(47):18769-74. https://doi.org/10.1073/pnas.1309934110

Development of a new technique to study swimming male gametes, and insights into their mating behaviours.

Carter L. M., Kafsack B. F. C., Llinás M., Mideo N., Pollitt L. C. & Reece S. E. (2013) Stress and Sex in Malaria Parasites: Why Does Commitment Vary? Evolution, Medicine, and Public Health, 2013(1):135-47. https://doi.org/10.1093/emph/eot011

Applying evolutionary theory to explain why parasite vary their level of investment into gametocytes (sexual stages) during infectgions

Pollitt L. C., Churcher T. S., Dawes E. J., Khan S. M., Sajid M., Basáñez M. G., Colegrave N. & Reece S. E. (2013) Costs of crowding for the transmission of malaria parasites. Evolutionary Applications, 6(4):617-29. https://doi.org/10.1111/eva.12048

Demonstrates that parasites show density dependence in the productivity and virulence of malaria infections in mosquitoes.

Mideo N., Reece S. E., Smith A. and Metcalf C.J.E. (2013) The Cinderella Syndrome: Why do malaria-infected cells burst at midnight? Trends in Parasitology, 29(1):10-6. https://doi.org/10.1016/j.pt.2012.10.006

Discusses the potential advantages to the host and the parasite of daily rhythms in parasite development.

2012

Ramiro R. S., Reece S. E. & Obbard D. J. (2012) Molecular evolution and phylogenetics of rodent malaria parasites. BMC Evolutionary Biology, 12(1):219. https://doi.org/10.1186/1471-2148-12-219

Creates a phylogeny (family tree) of rodent malaria species.

Khan S. M.,Reece S. E., Waters A. P., Janse C. J. and Kaczanowski S. (2012) Why are male malaria parasites in such a rush? Sex-specific evolution and host-parasite interactions. Evolution, Medicine, and Public Health, 2013(1):3-13. https://doi.org/10.1093/emph/eos003

Reveals that genes expressed exclusively in male gametocytes evolve more quickly than those in females.

Schneider P., Bell A. S., Sim D. G., O'Donnell A. J., Blanford S., Paaijmans K. P., Read A. F. and Reece S. E. (2012) Virulence, drug sensitivity and transmission success in the rodent malaria, Plasmodium chabaudi. Proceedings of the Royal Society of London Series B. 279(1747):4677-85. https://doi.org/10.1098/rspb.2012.1792

Drug treatment selects for the evolution of more harmful parasite strains.

Cameron A., Reece S. E., Drew D. R., Haydon D. T. & Yates A. J. (2012) Plasticity in transmission strategies of the malaria parasite, Plasmodium chabaudi: environmental and genetic effects. Evolutionary Applications, 6(2):365-76. https://doi.org/10.1111/eva.12005

Shows that parasite investment in gametocytes (sexual stages) correlates with host anaemia and varies across parasite strains.

Pollitt L. C., Reece S. E., Mideo N., Nussey D. H. & Colegrave N. (2012) The problem of autocorrelation in parasitology. PLoS Pathogens, 8(4):e1002590. https://doi.org/10.1371/journal.ppat.1002590

Illustrates that incorrect biological inference can result from analysing parasite dynamics during infections when temporal autocorrelation is not controlled for.

Mideo N., Acosta-Serrano A., Aebischer T., Brown M. J. F., Fenton A., Friman V-P., Restif O., Reece S. E., Webster J. P. & Brown S. P. (2012) Life in cells, hosts, and vectors: parasite evolution across scales. Infection, Genetics & Immunity, 13:344-7. https://doi.org/10.1016/j.meegid.2012.03.016

Summarises diverse studies to illustrate how parasite fitness is determined by processes acting across different levels of biological organization.

Staszewski V., *Reece S. E., O'Donnell A. J. and Cunningham E. J. A. (2012) Drug treatment of malaria infections can reduce levels of protection transferred to offspring via maternal immunity. Proceedings of the Royal Society of London B, 279(1737):2487-96. https://doi.org/10.1098/rspb.2011.1563

Shows that giving antimalarial drugs to pregnant mice can make their offspring more vulnerable to malaria than if mothers are untreated.

Mideo N. and Reece S. E. (2012) Plasticity in parasite phenotypes: evolutionary and ecological implications for disease. Future Microbiology, 7(1):17-24. https://doi.org/10.2217/fmb.11.134

Outlines work from the lab showing that parasites have flexible strategies that help them maintain fitness in the changing environment they experience inside the host.

2011

Reece S. E., Pollitt L. C., Colegrave N. and Gardner A. (2011) The meaning of death: evolution and ecology of apoptosis in protozoan parasites. PLoS Pathogens, 7(12): e1002320. https://doi.org/10.1371/journal.ppat.1002320

Outlines circumstances in which a suicide of parasites is consistent with Darwinian ‘survival of the fittest’

Mideo N., Savill N. J., Chadwick W., Schneider P., Read A. F., Day T. and Reece S.E. (2011) Causes of variation in malaria infection dynamics: insights from theory and data. American Naturalist, 178(6):174-88. https://doi.org/10.1086/662670Supplementary information A and Supplementary information B.

Combines mathematical models and data to explore whether variation in traits that underpin how parasites exploit their host can explain why some parasite strains are more harmful than others.

Mideo N., Nelson W.A., Reece S.E., Bell A.S, Read A.F. and Day T. (2011) Bridging Scales in the Evolution of Infectious Disease Life Histories: Application. Evolution, 65(11):3298-310. https://doi.org/10.1111/j.1558-5646.2011.01382.x

Combines mathematical models and data to link within-infection processes to population (epidemiological) processes to predict parasite evolution.

Innocent T.M., West S.A., Sanderson J.L., Hyrkkanen N. and Reece S.E. (2011) Lethal combat over limited resources: testing the importance of competitors and kin. Behavioural Ecology, 22(5):923-31. https://doi.org/10.1093/beheco/arq209

Parasitoid wasp paper: examines ecological and evolutionary forces that favour extreme aggression between relatives

Kaczanowski S., Sajid M. and Reece S.E. (2011) The evolution of apoptosis-like programmed cell death in unicellular protozoan parasites. Parasites & Vectors, 4(1):44. https://doi.org/10.1186/1756-3305-4-44

Explores the evolutionary history of genes associated with ‘suicide’ in single celled parasites.

Pollitt L.C., MacGregor P., Matthews K. and Reece S.E. (2011) Malaria and trypanosome transmission: different parasites, same rules? Trends in Parasitology, 27(5):197-203. https://doi.org/10.1086/658175

Applies evolutionary theory to predict how within-host environment influences the trade-off between survival and transmission in different parasite taxa.

Pollitt L.C., Mideo N.L., Drew D.R., Schneider P., Colegrave N., Khan S.M., Sajid M. and Reece S.E. (2011) Competition and the evolution of reproductive restraint in malaria parasites. American Naturalist, 177(3):358-67. https://doi.org/10.1086/658175

Reveals that parasites respond to the presence of competing strains in the host by reducing investment in sexual stages in the manner predicted to increase their competitive ability.

Ramiro R.S., Alpedrinha J., Carter L., Gardner A and Reece S.E. (2011) Sex and death: the effects of innate immune factors on the sexual reproduction of malaria parasites. PLoS Pathogens, 7(3):e1001309. https://doi.org/10.1371/journal.ppat.1001309

Shows that host immune factors affect the survival and fertility of male and female transmission stages in different ways and develops theory to predict how these effects shape the evolution of parasite reproductive strategies.

Abbot et al. with 137 authors. (2011) Inclusive fitness theory and eusociality. Nature, 471(7339):E1. https://doi.org/10.1038/nature09831

Comment arguing that understanding relatedness between interacting organisms provides insight into the evolution of social behaviours.

Culleton R.L., Inoue M., Reece S.E., Cheeseman S. and Carter R. (2011) Strain-specific immunity to the pre-erythrocytic stages of Plasmodium chabaudi. Parasite Immunology, 33(1):73-8. https://doi.org/10.1111/j.1365-3024.2010.01251.x

Demonstrates that immunity to incoming parasites, injected from the mosquito, is strongest against strains the host has already been exposed to.

O'Donnell A.J., Schneider P., McWatters H.G. and Reece S.E. (2011) The fitness costs of disrupting circadian rhythms in malaria parasites. Proceedings of the Royal Society London B. 278(1717):2429-36. https://doi.org/10.1098/rspb.2010.2457 Faculty of 1000 evaluation (recommended); Nature Research Highlight (Microbiology)

Modernised the study of ‘periodicity’ in malaria infection and provided a rare demonstration of the fitness benefits of rhythmic behaviour. Specifically, reveals that parasite fitness (in host survival and transmission potential) is enhanced when Plasmodium’s IDC rhythm is in synchrony with the host’s circadian rhythms.

2010

Pollitt L.C., Colegrave N., Khan S.M., Sajid M. and Reece S.E. (2010) Investigating the evolution of apoptosis in malaria parasites: the importance of ecology. Parasites & Vectors, 3(1):105. https://doi.org/10.1186/1756-3305-3-105

Outlines evolutionary explanations for why parasites might commit ‘suicide’ and illustrates the difficulties of testing these ideas.

Reece S.E., Ali E., Schneider P. and Babiker H.A. (2010) Stress, drugs and the evolution of reproductive restraint in malaria parasites. Proceedings of the Royal Society B, 277(1697):3123-9. https://doi.org/10.1098/rspb.2010.0564

Drug-sensitive, but not drug-resistant, human malaria parasites decrease their investment in sexual stages when exposed to low doses of drugs, showing parasites respond to changes in their proliferation rate rather the presence of drugs.

Abe J., Innocent T.M., Reece S.E. and West S.A. (2010) Virginity and the clutch size behaviour of a parasitoid wasp. Behavioural Ecology, 21(4):730-8. https://doi.org/10.1093/beheco/arq046

Parasitoid wasp paper: shows that females can determine whether other females competing for the same resources have mated or not.

Innocent T.M., Abe J., West S.A. and Reece S.E. (2010) Competition between relatives and the evolution of dispersal. Journal of Evolutionary Biology, 23(7):1374-85. https://doi.org/10.1111/j.1420-9101.2010.02015.x

Parasitoid wasp paper: examines how different levels of competition for resources between related and non-related females influence the dispersal rate of their offspring.

2009

Savill N.J., Chadwick W. and Reece S.E. (2009) Quantitative analysis of mechanisms that govern red blood cell age structure and dynamics during anaemia. PLoS Computational Biology, 5(6):e1000416. https://doi.org/10.1371/journal.pcbi.1000416

Combines mathematical models and data to evaluate hypotheses for maintaining equilibrium in red blood cell populations.

Reece S.E., Ramiro R.S. and Nussey D.H.N. (2009) Plastic parasites: sophisticated strategies for survival and reproduction? Evolutionary Applications, 2(1): 11-23. https://doi.org/10.1111/j.1752-4571.2008.00060.x.

Discusses the evolution of flexible strategies for surviving in the host and transmitting to mosquitoes.

2008

Schneider P., Chan B.H.K, Reece S.E. and Read A.F. (2008). Does the drug sensitivity of malaria parasites depend on their virulence? Malaria Journal, 7(1):257. https://doi.org/10.1186/1475-2875-7-257Commentary Stein (Trends in Parasitology)

More harmful parasite strains are better able to survive treatment with antimalarial drugs.

Reece S.E. and Thompson J. (2008) Transformation of the rodent malaria parasite, Plasmodium chabaudi and generation of stable fluorescent lines. Malaria Journal, 6(4):553. https://doi.org/10.1038/nprot.2011.313

Demonstrates that the rodent malaria P. chabaudi can be genetically modified.

Babiker H.A., Schneider P. and Reece S.E. (2008) Gametocytes: Insights gained during a decade of molecular monitoring. Trends in Parasitology, 24(11):525-30. https://doi.org/10.1016/j.pt.2008.08.001

Reviews recent discoveries made about the production and sex ratio of sexual, transmission, stages.

Reece S.E., Drew D.R. and Gardner A. (2008) Sex ratio adjustment and kin discrimination in malaria parasites. Nature, 453(7195):609. https://doi.org/10.1038/nature06954Supplementary info Faculty of 1000 evaluation (must read); Commentaries: Schall (Nature); Knowles and Sheldon (Current Biology); Schall(Trends in Parasitology).

Demonstrates that evolutionary theory developed to explain the biology of multicellular organisms can be applied to reveal how ‘sophisticated’ parasite strategies are. Specifically, reveals that Plasmodium can discriminate the relatedness of co-infecting genotypes and use this information to plastically adjust investment into male versus female transmission stages to maximise fitness.

2007

Drew D.R. and Reece S.E. (2007) Development of reverse transcription PCR techniques to analyse the density and sex ratio of gametocytes in genetically diverse Plasmodium chabaudi infections. Molecular and Biochemical Parasitology, 156(2):199-209. https://doi.org/10.1016/j.molbiopara.2007.08.004

Presents new methods to quantify the numbers of male and female transmission stages for the rodent malaria species, P. chabaudi.

Reece S.E., Innocent T.M. and West S.A. (2007) Lethal combat in the parasitoid, Melittobia acasta: are size and competitive environment important? Animal Behaviour, 74(5):1163-9. https://doi.org/10.1016/j.anbehav.2006.10.027

Parasitoid wasp paper: examines individual and ecological factors shaping the evolution of extremely aggressive behaviour.

Innocent T.M., West S.A. and Reece S.E. (2007) Lethal male-male combat and sex ratio evolution in a parasitoid wasp. Behavioural Ecology, 18(4):709-15. https://doi.org/10.1093/beheco/arm034

Parasitoid wasp paper: examines whether lethal combat between closely related males over access to mates explains the unusual sex ratios observed in this species.

Augustijn K.D., Kleemann R., Thompson J., Kooistra T., Crawford C.E., Reece S.E., Pain A., Siebum A.H.G., Janse C.J. and Waters A.P. (2007) Functional characterization of the Plasmodium homologue of Macrophage Migration Inhibitory Factor. Infection & Immunity, 75(3): 1116-1128. https://doi.org/10.1128/IAI.00902-06.

Examines whether malaria parasites produce a molecule that mimics part of the host’s immune response to manipulate the action of immune responses against the parasite.

Shuker D.M., Reece S.E., Lee A., Graham A., Duncan A.B. and West S.A. (2007) Information use in space and time: sex allocation behaviour in the parasitoid wasp Nasonia vitripennis. Animal Behaviour, 73(6):971-7. https://doi.org/10.1016/j.anbehav.2006.07.013

Parasitoid wasp paper: demonstrates that females are able to evaluate the number of other females competing for resources.

2005

Reece S.E., Wherry R.N. and Bloor J.M.G. (2005) Sex allocation and interactions between relatives in the bean beetle, Callosobruchus maculatus. Biological Processes, 70(3):282-8. https://doi.org/10.1016/j.beproc.2005.08.002

Beetle paper: examines whether females adjust the sex ratio of their offspring in the manner predicted by evolutionary theory.

Shutler D., Reece S.E., Mullie A., Billingsly P.F. and Read A.F. (2005) Rodent malaria parasites Plasmodium chabaudi and P. vinckei do not increase rates of gametocytogensis in reponse to mosquito probing. Proceedings of the Royal Society B, 272(1579):2397-402. https://doi.org/10.1098/rspb.2005.3232

Reveals that, contrary to expectation, parasites do not preferentially invest into transmission when mosquitos are available to vector them.

Shuker D.M., Pen I., Duncan A.B., Reece S.E. and West S.A. (2005) Sex ratios under asymmetrical local mate competition: theory and a test with parasitoid wasps. American Naturalist, 166(3):301-16. https://doi.org/10.1086/432562

Parasitoid wasp paper: shows that females consider the state of their local environment before making decisions about what offspring sex ratio to produce.

Reece S.E., Duncan A.B., West S.A. and Read A.F. (2005) Host cell preference and variable transmission strategies in malaria parasites. Proceedings of the Royal Society B, 272(1562):511-7. https://doi.org/10.1098/rspb.2004.2972

Demonstrates that parasite species respond differently to host anaemia in terms of their investment in sexual, transmission, stages.

2004

Shuker D.M., Reece S.E., Whitehorn P.R. and West S.A. (2004) Sib-mating does not lead to facultative sex ratio adjustment in the parasitoid wasp, Nasonia vitripennis. Evolutionary Ecology Research, 6(3):473-80. http://hdl.handle.net/1893/22805

Parasitoid wasp paper: demonstrates that females are not able to discriminate brothers from unrelated mates when making reproductive decisions.

Shuker D.M., Reece S.E., Taylor J.A.L. and West S.A. (2004) Wasp sex ratio behaviour when females on a patch are related. Animal Behaviour, 68(2):331-6. https://doi.org/10.1016/j.anbehav.2003.12.003

Parasitoid wasp paper: demonstrates that females are not able to discriminate sisters from non-kin when making reproductive decisions.

Reece S.E., Shuker D.M., Pen I., Duncan A.B., Choudhary A., Batchelor C.M. and West S.A. (2004) Kin discrimination and sex ratios in a parasitoid wasp. Journal of Evolutionary Biology, 17(1):208-16. https://doi.org/10.1046/j.1420-9101.2003.00640.x

Parasitoid wasp paper: demonstrates that females are not able to discriminate brothers from unrelated mates when making reproductive decisions.

2003

Reece S.E., Duncan A.B., West S.A. and Read A.F. (2003) Sex ratios in the rodent malaria parasite, Plasmodium chabaudi. Parasitology, 127(5):419-25. https://doi.org/10.1017/S0031182003004013Colour figures

Demonstrates that traditional methods for sexing male and female transmission stages can overestimate the proportion that are females and quantifies sex-specific mortality rates.

West S.A., Reece S.E. and Read A.F. (2003) Toxoplasma gondii, Sex and premature rejection. Trends in Parasitology, 19(4):155-7. https://doi.org/10.1016/S1471-4922(03)00033-3

Reply to comment on Evolution of gametocyte sex ratios in malaria and related apicomplexan (protozoan) parasites.

Gardner A., Reece S.E., and West S.A. (2003) Even more extreme fertility insurance and the sex ratios of protozoan blood parasites. Journal of Theoretical Biology, 223(4):515-21. https://doi.org/10.1016/S0022-5193(03)00142-5

Develops theory to predict how parasites should invest in male versus female transmission stages according to the fecundity of males and overall numbers of sexual stages.

2002

Reece S.E., Broderick A.C., Godley B.J. and West S.A. (2002) The effects of incubation environment, sex and pedigree on hatchling phenotype in a natural population of loggerhead sea turtles. Evolutionary Ecology Research, 4(5):737-48.

Tests evolutionary theory to explain why the sex of sea turtles is determined by temperature.

West S.A., Reece S.E. and Sheldon B.C. (2002) Sex ratios. Heredity, 88(2):117. https://doi.org/10.1038/sj.hdy.6800018

Outlines the state of affairs of research into offspring sex ratios.

2001

Godley B.J., Broderick A.C., Downie J.R., Glen F., Hays G.C., Houghton J., Kirkwood I. and Reece S.E. (2001) Thermal conditions in nests of loggerhead turtles: further evidence suggesting skewed sex ratios of hatchling production in the Mediterranean. Journal of Experimental Marine Biology and Ecology, 263(1):45-63. https://doi.org/10.1016/S0022-0981(01)00269-6

Details patterns of temperature fluctuations in sea turtle nests and the links with hatching success and sex ratio.

West S.A., Reece S.E. and Read A.F. (2001) Evolution of gametocyte sex ratios in malaria and related apicomplexan (protozoan) parasites. Trends in Parasitology, 17(11):525-31. https://doi.org/10.1016/S1471-4922(01)02058-X

Reviews research into the ratio of male to female sexual stages and explores evolutionary explanations for why a high proportion of females is common.

2000

Reece S.E. and Read A.F. (2000) Malaria sex ratios. Trends in Ecology & Evolution, 15(7):259-60. http://dx.doi.org/10.1016/S0169-5347(00)01893-0

Comment on research showing that parasites adjust the ratio of male to female sexual stages in response to host anaemia.

Broderick A.C., Godley B.J., Reece S.E. and Downie J.R. (2000) Incubation periods and sex ratios of green turtles: highly female biased hatchling production in the eastern Mediterranean. Marine Ecological Proceedings, 202:273-81. https://doi.org/10.3354/meps202273.

Estimates the sex ratios of sea turtle hatchlings and characterises the relationship between temperature and sex ratio.