Elsevier

Current Opinion in Insect Science

Volume 28, August 2018, Pages 113-117
Current Opinion in Insect Science

Do avian malaria parasites reduce vector longevity?

https://doi.org/10.1016/j.cois.2018.08.001Get rights and content

Highlights

  • •

    Avian malaria parasites are commonly found infecting birds in all continents, excluding Antarctica.

  • •

    Few studies have analysed the impact of these parasites on vector survival, often using unnatural host-parasite assemblages and reaching completely different conclusions.

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    The vector’s nutritional status and gut microbiota can explain some of these differences.

  • •

    More realistic experiments reproducing the range of conditions found under natural conditions are needed to understand the true impact of these parasites on vector survival.

Avian Plasmodium and malaria-like parasites of the genus Haemoproteus are widespread vector-borne parasites commonly found infecting birds. These parasites impose deleterious effects on their vertebrate hosts compromising their survival. While the interaction between these parasites and their vertebrate hosts has received much attention, the study of those factors determining the consequences of parasite infections in the insect vectors has been traditionally neglected. Recent studies have shown that host’s parasite load and the mosquito’s nutritional status and microbiota modulate the impact of parasites on mosquito longevity. Here, we provide a critical review of these studies to identify gaps in current knowledge and propose future research directions. Further experimental studies are needed to reveal the impact of avian malaria parasites in mosquitoes using realistic conditions found in wild parasite-mosquito assemblages.

Introduction

Avian haemosporidians (phylum: Apicomplexa) are blood parasites infecting birds that are transmitted by insect vectors [1]. Mosquitoes, especially those of the genus Culex, are the main vectors of the avian malaria parasites of the genus Plasmodium, although other genera including Anopheles, Aedes and Lutzia may also be involved in their transmission [2]. In addition to Plasmodium parasites, birds are commonly infected by the related malaria-like parasite Haemoproteus. Both parasite genera have a similar life cycle but differ in the vectors involved in their transmission, where sexual reproduction of the parasite occurs. Contrary to the case of Plasmodium parasites, Haemoproteus of the subgenus Parahaemoproteus are transmitted by biting midges Culicoides (Ceratopogoniidae) while louse flies act as vectors for the subgenus Haemoproteus. After an insect vector bites an infected host, parasite gametocytes develop into gametes in the insect midgut and fuse as zygotes to form ookinetes. Subsequently, parasites penetrate into the insect midgut wall where ookinetes develop into oocytes to form sporozoites, the infective form of the parasites. Parasite sporozoites invade the salivary gland of the insect vector where they accumulate until their inoculation to a new host in the following blood meal. Parasite development in the insect vectors usually takes from 8 to 22 days, although Haemoproteus sporozoites have been found in the salivary glands of Culicoides at 5 days post exposure (dpe) [1,3].

By definition, parasites reduce the fitness of their hosts [4]. However, evolutionary theory predicts differential parasite virulence (i.e. the damage done to the host) according to the mode of parasite transmission [5]. In vector-borne parasites, virulence may be different in the vertebrate host and the insect vector [6]. In spite of that, vectors may also suffer an important cost of infections in terms of fecundity and survival [7••], although the impact of avian malaria and malaria-like parasites in the survival of their insect vectors remains an open question.

Section snippets

Current knowledge

During the last few years, different studies have provided evidence of the costs of avian malaria and malaria-like infections in their insect vectors, including studies on the interaction between Plasmodium and mosquitoes [[13•],9••] as well as Haemoproteus infecting biting midges [10, 11, 12] and louse flies [13•] (Table 1). However, contradictory results have been frequently reported, with non-significant effects of parasite infections on mosquito longevity [14,15] or, even, infected

Parasite load in the vertebrate host

Gametocytaemia in birds, defined as the proportion of red blood cells (RBC) infected by gametocytes, is considered a major determinant of the success of malaria parasite development in the vector [17]. However, an elevated gametocytaemia (or parasitaemia) may also increase vector mortality [7••,9••], which becomes evident soon after exposure to infection [10]. In extreme cases, where insect vectors feed on blood from highly infected birds (5.2% gametocytaemia), mortality was 98% only twelve

The vector’s nutritional status

Host immune responses to fight off parasite infections are energetically costly with nutrition, among other factors, representing a main factor modulating these responses [21]. However, the role of nutritional stress modulating the cost of avian malaria infections in mosquitoes has been poorly studied. In their seminal paper, Ferguson and Read [7••] proposed the potential importance of controlling diet on studies on mosquito survival because infected mosquitoes use eight times as much glucose

Insect microbiota

Mosquito microbiota modulate the development of human malaria parasites in the vectors [26•] though mechanisms that include direct anti-parasite effects of microbiota on the parasite development [26•] or by stimulating the insect’s immune system [27]. Furthermore, mosquito microbiota may affect the impact of parasite infections on mosquito survival. In their study, Gendrin et al. [28] showed that antibiotic treated Anopheles gambiae were more susceptible to Plasmodium infections, suggesting

Concluding remarks and future directions

Avian Plasmodium and Haemoproteus impact the longevity of their vectors, as supported by studies on mosquitoes, biting midges and louse flies. However, important discrepancies between studies have been reported. Here, we report evidence for the role of three major factors determining the impact of parasites on insect vectors, including the parasite load in the vertebrate host and mosquito-related factors (i.e. the nutritional stress, gut microbiota).

A number of different avian Plasmodium

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This study was supported by the Spanish Ministry of Economy and Competition and from the European Regional Development Fund (FEDER) [Grant Number: CGL2015-65055-P to JF], the Spanish Society of Ethology and Evolutionary Biology and the BBVA Foundation [2017 Leonardo Grant for Researchers and Cultural Creators to JMP]. The Foundation accepts no responsibility for the opinions, statements and contents included in the project and/or the results thereof, which are entirely the responsibility of the

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