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Ecological influences on the behaviour and fertility of malaria parasites.

Carter LM, Pollitt LC, Wilson LG, Reece SE - Malar. J. (2016)

Bottom Line: Male gametes need to locate and fertilize females in the challenging environment of the mosquito blood meal, but remarkably little is known about the ecology and behaviour of male gametes.Specifically, the data confirm that: (a) rates of male gametogenesis vary when induced by the family of compounds (tryptophan metabolites) thought to trigger gamete differentiation in nature; and (b) complex relationships between gametogenesis and mating success exist across parasite species.In addition, the data reveal that (c) microparticles of the same size as red blood cells negatively affect mating success; and (d) instead of swimming in random directions, male gametes may be attracted by female gametes.

View Article: PubMed Central - PubMed

Affiliation: Ashworth Laboratories, School of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, UK.

ABSTRACT

Background: Sexual reproduction in the mosquito is essential for the transmission of malaria parasites and a major target for transmission-blocking interventions. Male gametes need to locate and fertilize females in the challenging environment of the mosquito blood meal, but remarkably little is known about the ecology and behaviour of male gametes.

Methods: Here, a series of experiments explores how some aspects of the chemical and physical environment experienced during mating impacts upon the production, motility, and fertility of male gametes.

Results and conclusions: Specifically, the data confirm that: (a) rates of male gametogenesis vary when induced by the family of compounds (tryptophan metabolites) thought to trigger gamete differentiation in nature; and (b) complex relationships between gametogenesis and mating success exist across parasite species. In addition, the data reveal that (c) microparticles of the same size as red blood cells negatively affect mating success; and (d) instead of swimming in random directions, male gametes may be attracted by female gametes. Understanding the mating ecology of malaria parasites, may offer novel approaches for blocking transmission and explain adaptation to different species of mosquito vectors.

No MeSH data available.


Related in: MedlinePlus

Variation in response to GAFs of Plasmodium yoelii subspecies. Responses of P. yoelii subspecies (Pyn: P. yoelii nigeriensis; Pys: P. yoelii subspecies; and Pyy: P. yoelii yoelii) to GAFs at 10−4 M (XA: xanthurenic acid; KA: kynurenic acid; and Tryp: tryptophan). a Mean ± SEM log2 + 0.001 transformed densities of exflagellating males relative to the pH 8 control. b Mean ± SEM log2 transformed densities of ookinetes. Zeros indicate combinations where no ookinetes were observed. N ranges from 3 to 5 independent infections for each GAF
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Fig3: Variation in response to GAFs of Plasmodium yoelii subspecies. Responses of P. yoelii subspecies (Pyn: P. yoelii nigeriensis; Pys: P. yoelii subspecies; and Pyy: P. yoelii yoelii) to GAFs at 10−4 M (XA: xanthurenic acid; KA: kynurenic acid; and Tryp: tryptophan). a Mean ± SEM log2 + 0.001 transformed densities of exflagellating males relative to the pH 8 control. b Mean ± SEM log2 transformed densities of ookinetes. Zeros indicate combinations where no ookinetes were observed. N ranges from 3 to 5 independent infections for each GAF

Mentions: The effect of each compound on exflagellation did not significantly differ between any of the P. yoelii subspecies (compound*subspecies: χ4,72 = 4.91, P = 0.297, Additional file 1: Table S2). However, the three subspecies (χ2,52 = 19.31, P < 0.001) showed significant differences in their exflagellation responses to the three GAF types (χ2,52 = 13.26, P = 0.001) (Fig. 3a). Exflagellation rates were higher for P. y. nigeriensis and P. yoelii subspecies than observed for P. y. yoelii (~2-fold lower). The response to GAFs followed the same pattern as for P. berghei: with the highest exflagellation in XA cultures and lowest in Tryp cultures. No ookinetes were observed in any cultures containing KA or Tryp across all subspecies, or for P. yoelii subspecies at pH 8. Zero ookinete counts for KA and Tryp may be due to post exflagellation inhibitory effects on the microgametes, female gametes, and/or zygotes, suggesting P. yoelii is more sensitive to inhibition than P. berghei.Fig. 3


Ecological influences on the behaviour and fertility of malaria parasites.

Carter LM, Pollitt LC, Wilson LG, Reece SE - Malar. J. (2016)

Variation in response to GAFs of Plasmodium yoelii subspecies. Responses of P. yoelii subspecies (Pyn: P. yoelii nigeriensis; Pys: P. yoelii subspecies; and Pyy: P. yoelii yoelii) to GAFs at 10−4 M (XA: xanthurenic acid; KA: kynurenic acid; and Tryp: tryptophan). a Mean ± SEM log2 + 0.001 transformed densities of exflagellating males relative to the pH 8 control. b Mean ± SEM log2 transformed densities of ookinetes. Zeros indicate combinations where no ookinetes were observed. N ranges from 3 to 5 independent infections for each GAF
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4835847&req=5

Fig3: Variation in response to GAFs of Plasmodium yoelii subspecies. Responses of P. yoelii subspecies (Pyn: P. yoelii nigeriensis; Pys: P. yoelii subspecies; and Pyy: P. yoelii yoelii) to GAFs at 10−4 M (XA: xanthurenic acid; KA: kynurenic acid; and Tryp: tryptophan). a Mean ± SEM log2 + 0.001 transformed densities of exflagellating males relative to the pH 8 control. b Mean ± SEM log2 transformed densities of ookinetes. Zeros indicate combinations where no ookinetes were observed. N ranges from 3 to 5 independent infections for each GAF
Mentions: The effect of each compound on exflagellation did not significantly differ between any of the P. yoelii subspecies (compound*subspecies: χ4,72 = 4.91, P = 0.297, Additional file 1: Table S2). However, the three subspecies (χ2,52 = 19.31, P < 0.001) showed significant differences in their exflagellation responses to the three GAF types (χ2,52 = 13.26, P = 0.001) (Fig. 3a). Exflagellation rates were higher for P. y. nigeriensis and P. yoelii subspecies than observed for P. y. yoelii (~2-fold lower). The response to GAFs followed the same pattern as for P. berghei: with the highest exflagellation in XA cultures and lowest in Tryp cultures. No ookinetes were observed in any cultures containing KA or Tryp across all subspecies, or for P. yoelii subspecies at pH 8. Zero ookinete counts for KA and Tryp may be due to post exflagellation inhibitory effects on the microgametes, female gametes, and/or zygotes, suggesting P. yoelii is more sensitive to inhibition than P. berghei.Fig. 3

Bottom Line: Male gametes need to locate and fertilize females in the challenging environment of the mosquito blood meal, but remarkably little is known about the ecology and behaviour of male gametes.Specifically, the data confirm that: (a) rates of male gametogenesis vary when induced by the family of compounds (tryptophan metabolites) thought to trigger gamete differentiation in nature; and (b) complex relationships between gametogenesis and mating success exist across parasite species.In addition, the data reveal that (c) microparticles of the same size as red blood cells negatively affect mating success; and (d) instead of swimming in random directions, male gametes may be attracted by female gametes.

View Article: PubMed Central - PubMed

Affiliation: Ashworth Laboratories, School of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, UK.

ABSTRACT

Background: Sexual reproduction in the mosquito is essential for the transmission of malaria parasites and a major target for transmission-blocking interventions. Male gametes need to locate and fertilize females in the challenging environment of the mosquito blood meal, but remarkably little is known about the ecology and behaviour of male gametes.

Methods: Here, a series of experiments explores how some aspects of the chemical and physical environment experienced during mating impacts upon the production, motility, and fertility of male gametes.

Results and conclusions: Specifically, the data confirm that: (a) rates of male gametogenesis vary when induced by the family of compounds (tryptophan metabolites) thought to trigger gamete differentiation in nature; and (b) complex relationships between gametogenesis and mating success exist across parasite species. In addition, the data reveal that (c) microparticles of the same size as red blood cells negatively affect mating success; and (d) instead of swimming in random directions, male gametes may be attracted by female gametes. Understanding the mating ecology of malaria parasites, may offer novel approaches for blocking transmission and explain adaptation to different species of mosquito vectors.

No MeSH data available.


Related in: MedlinePlus