Spring reproductive success influences autumnal malarial load in a passerine bird

Although avian haemosporidian parasites are widely used as model organisms to study fundamental questions in evolutionary and behavorial ecology of host-parasite inter- actions, some of their basic characteristics, such as seasonal variations in within-host density, are still mostly unknown. In addition, their interplay with host reproductive suc- cess in the wild seems to depend on the interaction of many factors, starting with host and parasite species and the temporal scale under study. Here, we monitored the par- asitemia of two haemosporidian parasites – Plasmodium relictum (lineage SGS1) and P. homonucleophilum (lineage SW2) – in two wild populations of great tits (Parus major) in Switzerland over three years, to characterize their dynamics. We also collected data on birds’ reproductive output – laying date, clutch size, fledging success – to determine whether they were associated with parasitemia before (winter), during (spring) and after (autumn) breeding season. Parasitemia of both species dramatically increased in spring, in a way that was correlated to parasitemia in winter. Parasitemia before and during breeding season did not explain reproductive success. However, the birds which fledged the more chicks had higher parasitemia in autumn, which was not associated with their parasitemia in previous spring. Our results tend to indicate that high haemosporidian parasite loads do not impair reproduction in great tits, but high resource allocation into reproduction can leave birds less able to maintain low parasitemia over the following months

Different distribution of malaria parasite in left and right extremities of vertebrate hosts translates into differences in parasite transmission

International audienceMalaria, a vector-borne disease caused by Plasmodium spp., remains a major global cause of mortality. Optimization of disease control strategies requires a thorough understanding of the processes underlying parasite transmission. While the number of transmissible stages (gametocytes) of Plasmodium in blood is frequently used as an indicator of host-to-mosquito transmission potential, this relationship is not always clear. Significant effort has been made in developing molecular tools that improve gametocyte density estimation and therefore prediction of mosquito infection rates. However a significant level of uncertainty around estimates remains. The weakness in the relationship between gametocyte burden, measured from a blood sample, and the mosquito infection rate could be explained by a non-homogeneous distribution of gametocytes in the bloodstream. The estimated gametocyte density would then only be a single snapshot that does not reflect the host infectivity. This aspect of Plasmodium infection, however, remains largely neglected. In both humans and birds, we found here that the gametocyte densities differed depending on which side of the body the sample was taken, suggesting that gametocytes are not homogeneously distributed within the vertebrate host. We observed a fluctuating asymmetry, in other words, the extremity of the body with the highest density of parasites is not always the same from one individual to another. An estimation of gametocyte density from only one blood sample, as is commonly measured, could, therefore, over-or underestimated the infectivity of gametocyte carriers. This might have important consequences on the epidemiology of the disease since we show that this variation influences host-to-mosquito transmission. Vectors fed on the least infected body part had a lower parasite burden than those fed on the most infected part. The heterogeneous distribution of gametocytes in bloodstream should be considered to improve diagnosis and test new malaria control strategies

Evolutionary ecology of the host / mosquito / Plasmodium interaction : sources of heterogeneity of vectors' infection

Les moustiques jouent un rôle essentiel dans la dynamique de transmission du paludisme. Plusieurs traits d’histoire de vie de ces insectes hématophages vont, en effet, intervenir dans le calcul du taux reproductif de base du parasite. Parmi eux, la probabilité et l’intensité d’infection des vecteurs, suite à la prise d’un repas de sang infectieux, sont des facteurs primordiaux pour la transmission de Plasmodium. Pourtant, au sein d'une même population, une réelle hétérogénéité d’infection des moustiques a été observée: alors que certain ne sont pas infectés, que d'autres le sont faiblement, une partie des vecteurs vont présenter des taux d'infection extrêmement forts. Identifier les sources de variations responsables de cette hétérogénéité est indispensable pour comprendre la dynamique de transmission de Plasmodium. Certains paramètres d’origine génétique et environnementale, tel que la température et la nutrition, ont déjà clairement été identifiés comme ayant un impact sur le taux d’infection des moustiques. Néanmoins, de nombreux facteurs restent encore à explorer. En utilisant un système expérimental composé du parasite de la malaria aviaire Plasmodium relictum, de son vecteur naturel le moustique Culex pipiens et de l’un de ses hôtes vertébrés Serinus canaria, nous nous sommes intéressés aux effets de certains de ces paramètres, peu pris en compte jusqu’à présent, sur l’infection des moustiques. Nous avons notamment pu mettre en évidence des conséquences importante de l’infection parentale, de l’âge des vecteurs, ainsi que de leur fond génétique. Parallèlement, nous nous sommes intéressés à un facteur souvent laissé de côté, l’effet « hôte vertébré » sur l’infection des moustiques. Dans cette dernière partie, on a pu observer que la dynamique d’infection du parasite au sein de l’hôte influence de manière importante le taux de transmission de Plasmodium. Les sources d’hétérogénéité d’infections des moustiques sont donc multiples et l’ensemble des membres de cette association tripartite hôte/parasite/vecteur vont pouvoir influencer de manière importante la dynamique de transmission du parasite.Mosquitoes play a key role in the dynamics of malaria transmission. Indeed, several life history traits of these bloodsucking insects are closely associated with the basic reproductive rate of the malaria parasite. One of the most important parameters for the transmission of Plasmodium is the rate and intensity of the mosquito infection. However, within a single population, a great heterogeneity of mosquito infection levels is often observed: some mosquitoes are not infected, others are only weakly infected, and yet others have extremely high infection rates. Identifying the sources of variation responsible for this heterogeneity is essential in order to understand the transmission dynamics of Plasmodium. Certain genetic and environmental (temperature, nutrition) parameters have already been identified as having an impact on mosquito infection rates. Nevertheless, many factors remain to be explored. Using an experimental system composed of the avian malaria parasite Plasmodium relictum, its natural vector Culex pipiens and one of its vertebrate host Serinus canaria, we have investigated the effect of several seldom investigated parameters on the infection of mosquitoes. We observed surprising effects of the effect of parental infection, mosquito age and genetic background. In parallel, we also studied a rarely investigated parameter: the impact of the vertebrate host on the mosquito infection rate. We showed that parasite infection dynamics within the host, at short but also long time scales, significantly influence the transmission of Plasmodium to the vector. The sources of heterogeneity of mosquito infection are therefore multiple and all members of this tripartite partnership (i.e. host / parasite / vector) are able to significantly influence the transmission dynamics of the parasite

Ecologie évolutive des interactions Hôte / Moustique / Plasmodium : sources d’hétérogénéité de l’infection des vecteurs

Mosquitoes play a key role in the dynamics of malaria transmission. Indeed, several life history traits of these bloodsucking insects are closely associated with the basic reproductive rate of the malaria parasite. One of the most important parameters for the transmission of Plasmodium is the rate and intensity of the mosquito infection. However, within a single population, a great heterogeneity of mosquito infection levels is often observed: some mosquitoes are not infected, others are only weakly infected, and yet others have extremely high infection rates. Identifying the sources of variation responsible for this heterogeneity is essential in order to understand the transmission dynamics of Plasmodium. Certain genetic and environmental (temperature, nutrition) parameters have already been identified as having an impact on mosquito infection rates. Nevertheless, many factors remain to be explored. Using an experimental system composed of the avian malaria parasite Plasmodium relictum, its natural vector Culex pipiens and one of its vertebrate host Serinus canaria, we have investigated the effect of several seldom investigated parameters on the infection of mosquitoes. We observed surprising effects of the effect of parental infection, mosquito age and genetic background. In parallel, we also studied a rarely investigated parameter: the impact of the vertebrate host on the mosquito infection rate. We showed that parasite infection dynamics within the host, at short but also long time scales, significantly influence the transmission of Plasmodium to the vector. The sources of heterogeneity of mosquito infection are therefore multiple and all members of this tripartite partnership (i.e. host / parasite / vector) are able to significantly influence the transmission dynamics of the parasite.Les moustiques jouent un rôle essentiel dans la dynamique de transmission du paludisme. Plusieurs traits d’histoire de vie de ces insectes hématophages vont, en effet, intervenir dans le calcul du taux reproductif de base du parasite. Parmi eux, la probabilité et l’intensité d’infection des vecteurs, suite à la prise d’un repas de sang infectieux, sont des facteurs primordiaux pour la transmission de Plasmodium. Pourtant, au sein d'une même population, une réelle hétérogénéité d’infection des moustiques a été observée: alors que certain ne sont pas infectés, que d'autres le sont faiblement, une partie des vecteurs vont présenter des taux d'infection extrêmement forts. Identifier les sources de variations responsables de cette hétérogénéité est indispensable pour comprendre la dynamique de transmission de Plasmodium. Certains paramètres d’origine génétique et environnementale, tel que la température et la nutrition, ont déjà clairement été identifiés comme ayant un impact sur le taux d’infection des moustiques. Néanmoins, de nombreux facteurs restent encore à explorer. En utilisant un système expérimental composé du parasite de la malaria aviaire Plasmodium relictum, de son vecteur naturel le moustique Culex pipiens et de l’un de ses hôtes vertébrés Serinus canaria, nous nous sommes intéressés aux effets de certains de ces paramètres, peu pris en compte jusqu’à présent, sur l’infection des moustiques. Nous avons notamment pu mettre en évidence des conséquences importante de l’infection parentale, de l’âge des vecteurs, ainsi que de leur fond génétique. Parallèlement, nous nous sommes intéressés à un facteur souvent laissé de côté, l’effet « hôte vertébré » sur l’infection des moustiques. Dans cette dernière partie, on a pu observer que la dynamique d’infection du parasite au sein de l’hôte influence de manière importante le taux de transmission de Plasmodium. Les sources d’hétérogénéité d’infections des moustiques sont donc multiples et l’ensemble des membres de cette association tripartite hôte/parasite/vecteur vont pouvoir influencer de manière importante la dynamique de transmission du parasite

Long-term pathogenic response to Plasmodium relictum infection in Culex pipiens mosquito.

The transmission of Plasmodium within a vertebrate host population is strongly associated with the life history traits of its vector. Therefore the effect of malaria infection on mosquito fecundity and longevity has traditionally received a lot of attention. Several species of malaria parasites reduce mosquito fecundity, nevertheless almost all of the studies have focused only on the first gonotrophic cycle. Yet, during their lifetime, female mosquitoes go through several gonotrophic cycles, which raises the question of whether they are able to compensate the fecundity costs induced by the parasite. The impact of Plasmodium infection on female longevity is not so clear and has produced conflicting results. Here we measured the impact of Plasmodium relictum on its vector's longevity and fecundity during three consecutive gonotrophic cycles. In accordance with previous studies, we observed a negative impact of Plasmodium infection on mosquito (Culex pipiens) fecundity in the first gonotrophic cycle. Interestingly, despite having taken two subsequent uninfected blood meals, the negative impact of malaria parasite persisted. Nevertheless no impact of infection on mosquito longevity was observed. Our results are not in line with the hypothesis that the reduction of fecundity observed in infected mosquitoes is an adaptive strategy of Plasmodium to increase the longevity of its vector. We discuss the different underlying mechanisms that may explain our results