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On the evolution of reproductive restraint in malaria.

ABSTRACT: Malaria is one of the leading causes of death among infectious diseases in the world, claiming over one million lives every year. By these standards, this highly complex parasite is extremely successful at generating new infections. Somewhat surprisingly, however, many malaria species seem to invest relatively little in gametocytes, converting only a small percentage of circulating asexual parasite forms into this transmissible form. In this article, we use mathematical models to explore three of the hypotheses that have been proposed to explain this apparent 'reproductive restraint' and develop a novel, fourth hypothesis. We find that only one of the previous three hypotheses we explore can explain such low gametocyte conversion rates, and this hypothesis involves a very specific form of density-dependent transmission-blocking immunity. Our fourth hypothesis also provides a potential explanation and is based on the occurrence of multiple infections and the resultant within-host competition between malaria strains that this entails. Further experimental work is needed to determine which of these two hypotheses provides the most likely explanation.

SUBMITTER: Mideo N

PROVIDER: S-EPMC2602685 | biostudies-other | 2008 May

REPOSITORIES: biostudies-other

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On the evolution of reproductive restraint in malaria.

Mideo Nicole N Day Troy T

Proceedings. Biological sciences 20080501 1639

Malaria is one of the leading causes of death among infectious diseases in the world, claiming over one million lives every year. By these standards, this highly complex parasite is extremely successful at generating new infections. Somewhat surprisingly, however, many malaria species seem to invest relatively little in gametocytes, converting only a small percentage of circulating asexual parasite forms into this transmissible form. In this article, we use mathematical models to explore three o ...[more]

PMID: 18303001

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Project description:During copulation, the major Afro-tropical malaria vector Anopheles gambiae s.s. transfers male accessory gland (MAG) proteins to females as a solid mass (i.e. the "mating plug"). These proteins are postulated to function as important modulators of female post-mating responses. To understand the role of selective forces underlying the evolution of these proteins in the A. gambiae complex, we carried out an evolutionary analysis of gene sequence and expression divergence on a pair of paralog genes called AgAcp34A-1 and AgAcp34A-2. These encode MAG-specific proteins which, based on homology with Drosophila, have been hypothesized to play a role in sperm viability and function.Genetic analysis of 6 species of the A. gambiae complex revealed the existence of a third paralog (68-78% of identity), that we named AgAcp34A-3. FISH assays showed that this gene maps in the same division (34A) of chromosome-3R as the other two paralogs. In particular, immuno-fluorescence assays targeting the C-terminals of AgAcp34A-2 and AgAcp34A-3 revealed that these two proteins are localized in the posterior part of the MAG and concentrated at the apical portion of the mating plug. When transferred to females, this part of the plug lies in proximity to the duct connecting the spermatheca to the uterus, suggesting a potential role for these proteins in regulating sperm motility. AgAcp34A-3 is more polymorphic than the other two paralogs, possibly because of relaxation of purifying selection. Since both unequal crossing-over and gene conversion likely homogenized the members of this gene family, the interpretation of the evolutionary patterns is not straightforward. Although several haplotypes of the three paralogs are shared by most A. gambiae s.l. species, some fixed species-specific replacements (mainly placed in the N- and C-terminal portions of the secreted peptides) were also observed, suggesting some lineage-specific adaptation.Progress in understanding the signaling cascade in the A. gambiae reproductive pathway will elucidate the interaction of this MAG-specific protein family with their female counterparts. This knowledge will allow a better evaluation of the relative importance of genes involved in the reproductive isolation and fertility of A. gambiae species and could help the interpretation of the observed evolutionary patterns.

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On the evolution of reproductive restraint in malaria.

Publications

On the evolution of reproductive restraint in malaria.

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