Last-come, best served? Mosquito biting order and Plasmodium transmission

International audienceA pervasive characteristic of parasite infections is their tendency to be overdispersed. Understanding the mechanisms underlying this overdispersed distribution is of key importance as it may impact the transmission dynamics of the pathogen. Although multiple factors ranging from environmental stochasticity to inter-individual heterogeneity may explain parasite overdispersion, parasite infection is also overdispersed in an inbred host population maintained under laboratory conditions, suggesting that other mechanisms are at play. Here, we show that the aggregated distribution of malaria parasites within mosquito vectors is partially explained by a temporal heterogeneity in parasite infectivity triggered by the bites of mosquitoes. Parasite transmission tripled between the mosquito's first and last blood feed in a period of only 3 h. Surprisingly, the increase in transmission is not associated with an increase in parasite investment in production of the transmissible stage. Overall, we highlight that Plasmodium is capable of responding to the bites of mosquitoes to increase its own transmission at a much faster pace than initially thought and that this is partly responsible for overdispersed distribution of infection. We discuss the underlying mechanisms as well as the broader implications of this plastic response for the epidemiology of malaria

Evolution of transgenerational immunity in invertebrates.

Over a decade ago, the discovery of transgenerational immunity in invertebrates shifted existing paradigms on the lack of sophistication of their immune system. Nonetheless, the prevalence of this trait and the ecological factors driving its evolution in invertebrates remain poorly understood. Here, we develop a theoretical host-parasite model and predict that long lifespan and low dispersal should promote the evolution of transgenerational immunity. We also predict that in species that produce both philopatric and dispersing individuals, it may pay to have a plastic allocation strategy with a higher transgenerational immunity investment in philopatric offspring because they are more likely to encounter locally adapted pathogens. We review all experimental studies published to date, comprising 21 invertebrate species in nine different orders, and we show that, as expected, longevity and dispersal correlate with the transfer of immunity to offspring. The validity of our prediction regarding the plasticity of investment in transgenerational immunity remains to be tested in invertebrates, but also in vertebrate species. We discuss the implications of our work for the study of the evolution of immunity, and we suggest further avenues of research to expand our knowledge of the impact of transgenerational immune protection in host-parasite interactions.This is the author accepted manuscript. The final version is available from Royal Society Publishing via http://dx.doi.org/10.1098/rspb.2016.113

Sex-biased parasitism in vector-borne disease: Vector preference?

Sex-biased infections are a recurrent observation in vertebrates. In many species, males are more parasitized than females. Two potentially complementary mechanisms are often suggested to explain this pattern: sexual differences in susceptibility mainly caused by the effect of sex hormones on immunity and differential exposure to parasites. Exposure is mostly a consequence of host behavioural traits, but vector-borne parasitic infections involve another degree of complexity due to the active role of vectors in transmission. Blood-sucking insects may make choices based on cues produced by hosts. Regarding malaria, several studies highlighted a male-biased infection by Plasmodium sp in great tits (Parus major). We hypothesize that the mosquito vector, Culex pipiens, might at least partially cause this bias by being more attracted to male birds. Intrinsic variation associated to bird sex would explain a preference of mosquitoes for males. To test this hypothesis, we provide uninfected mosquitoes with a choice between uninfected male and female nestlings. Mosquito choice is assessed by sex typing of the ingested blood. We did not observe any preference for a given sex. This result does not support our prediction of a preference of mosquitoes for male great tits during the nestling period. In conclusion, mosquitoes do not seem to have an intrinsic preference for male nestlings. However, sexually divergent traits (e.g. behaviour, odour, metabolic rate) present in adults may play a role in the attraction of mosquitoes and should be investigated

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

The effect of dietary antioxidant supplementation in a vertebrate host on the infection dynamics and transmission of avian malaria to the vector.

Host susceptibility to parasites is likely to be influenced by intrinsic factors, such as host oxidative status determined by the balance between pro-oxidant production and antioxidant defences. As a result, host oxidative status acts as an environmental factor for parasites and may constrain parasite development. We evaluated the role of host oxidative status on infection dynamics of an avian malarial parasite by providing canaries (Serinus canaria) with an antioxidant supplementation composed of vitamin E (a lipophilic antioxidant) and olive oil, a source of monounsaturated fatty acids. Another group received a standard, non-supplemented food. Half of the birds in each group where then infected with the haemosporidian parasite, Plasmodium relictum. We monitored the parasitaemia, haematocrit level, and red cell membrane resistance, as well as the transmission success of the parasite to its mosquito vector, Culex pipiens. During the acute phase, the negative effect of the infection was more severe in the supplemented group, as shown by a lower haematocrit level. Parasitaemia was lower in the supplemented group during the chronic phase only. Mosquitoes fed on supplemented hosts were more often infected than mosquitoes fed on the control group. These results suggest that dietary antioxidant supplementation conferred protection against Plasmodium in the long term, at the expense of a short-term negative effect. Malaria parasites may take advantage of antioxidants, as shown by the increased transmission rate in the supplemented group. Overall, our results suggest an important role of oxidative status in infection outcome and parasite transmission

Grandparental immune priming in the pipefish Syngnathus typhle

Background: Phenotypic changes in response to environmental influences can persist from one generation into the next. In many systems parental parasite experience influences offspring immune responses, known as transgenerational immune priming (TGIP). TGIP in vertebrates is mainly maternal and short-term, supporting the adaptive immune system of the offspring during its maturation. However, if fathers and offspring have a close physical connection, evolution of additional paternal immune priming can be adaptive. Biparental TGIP may result in maximized immunological protection. Here, we investigate multigenerational biparental TGIP in the sex-role reversed pipefish Syngnathus typhle by exposing grandparents to an immune challenge with heat-killed bacteria and assessing gene expression (44 target genes) of the F2-generation. Results: Grandparental immune challenge induced gene expression of immune genes in one-week-old grandoffspring. Similarly, genes mediating epigenetic regulation including DNA-methylation and histone modifications were involved in grandparental immune priming. While grand-maternal impact was strong on genes of the complement component system, grand-paternal exposure changed expression patterns of genes mediating innate immune defense. Conclusion: In a system with male pregnancy, grandparents influenced the immune system of their grandoffspring in a sex-specific manner, demonstrating multigenerational biparental TGIP. The involvement of epigenetic effects suggests that TGIP via the paternal line may not be limited to the pipefish system that displays male pregnancy. While the benefits and costs of grandparental TGIP depend on the temporal heterogeneity of environmental conditions, multigenerational TGIP may affect host-parasite coevolution by dampening the amplitude of Red Queen Dynamics

Host Specialization and Dispersal in Avian Haemosporidians

In order to be able to understand the ecological and evolutionary processes involved in the emergence of infectious diseases, one needs to comprehend how parasites arrive at new geographical areas and how they manage to maintain viable populations and even expand their ranges. We discuss host specificity in avian haemosporidians and how encounter and compatibility filters affect the dispersal of avian haemosporidians, and how these filters affect avian haemosporidian assemblages at different spatial and evolutionary scales. There are at least three important barriers to the dispersal of avian haemosporidians: (i) geographic barriers, (ii) environmental barriers, and (iii) interspecies barriers. In this chapter, we discuss the factors involved in these barriers and their effects on the structure of avian haemosporidian assemblages. Host specificity plays an important role in parasite dispersal, and in the case of avian haemosporidians that are vector-borne parasites, it needs to be evaluated both at the vector and bird host levels. Understanding the effects of these factors on host–vector–parasite dynamics is important to unravel the dispersal and diversification mechanisms of avian haemosporidians. We end this chapter reviewing host specialization in avian haemosporidians of tropical regions, discussing the mechanisms involved in the dispersal and specialization of these parasites and point out important research gaps that need attention