Trends in Parasitology
ReviewPopulation dynamics of Plasmodium sporogony
Section snippets
Parasite abundance wanes…then waxes
Malaria transmission hinges on the successful development of sexual-stage Plasmodium parasites within the insect vector – a process known as ‘sporogony’. Sporogony involves a sequence of morphologically distinct life-stages developing in specific anatomical locations within the insect [1]. The sequence is similar for all Plasmodium species, regardless of whether development occurs in anopheline mosquitoes (i.e. mammalian malaria), culicine mosquitoes (i.e. avian malaria) or phlebotomine sand
Sporogony from the viewpoint of population dynamics: a long history
All organisms exist as populations. The study of populations basically involves counting some or all of the organisms within one or more populations and using the resulting counts to estimate various parameters such as density, distribution, mortality, etc. The same general principles used to study free-living organisms can be applied to the study of Plasmodium populations developing within mosquitoes. In theory, the gametocytes infecting a single vertebrate host can be considered a population.
The kinetics of early sporogony differs among Plasmodium species
Events during early sporogony are transitory. Thus, to study the population dynamics of early sporogony it is important to know when to sample for parasites. In addition, early sporogony is intertwined with the kinetics of mosquito digestion [13]. During mosquito engorgement, blood is pumped by the cibarium (variously lined with cuticular teeth [14]) into the midgut. Within an hour, the blood meal becomes a paste as it congeals and excess water is removed by diuresis [15]. Several hours later,
Efficiency of life-stage transitions during early sporogony
Losses in parasite abundance between successive life-stages have been expressed using the relatively simple calculation of ‘killing powers’, or k values (Box 1), although more mathematically intensive analyses (e.g. population matrices) might also be applicable. Some studies on early sporogony quantified two life-stage transitions (gametocyte-to-ookinete and ookinete-to-oocyst) 22, 24, 35, 36, 37, 38, 39, 40. Other studies used monoclonal antibodies and immunofluorescent techniques to identify
Efficiency of life-stage transitions during late sporogony
There are fewer quantitative studies on the efficiency of late sporogony than early sporogony, perhaps because to perform such studies, sporozoites in the hemolymph must be separated from sporozoites within the salivary glands, and this requires more delicate techniques than simple midgut excision 24, 28. A mature Plasmodium oocyst can contain several thousand sporozoites [44]. However, time-course studies indicate that in many infections, not all mature oocysts present on a midgut necessarily
Changing patterns of aggregation during early sporogony
Anyone who has ever counted oocysts soon recognizes that oocysts are not distributed randomly among mosquitoes. Even in batches of mosquitoes infected simultaneously from the same host, most mosquitoes might contain few or no oocysts, whereas a minority of mosquitoes might contain many oocysts. This pattern of aggregation has been described mathematically as fitting the negative binomial distribution 45, 46, 47, 48 and is typical of most parasite populations [49]. In the case of mosquito
Future perspectives
Knowledge of the population dynamics of sporogony is fundamental to our understanding of Plasmodium biology, and can have practical applications. For example, stage-specific life tables (k values) reveal points of inefficiency in the sporogonic cycle that might be vulnerable to attack. Likewise, patterns of parasite aggregation indicate that host-to-host differences in infectivity to mosquitoes are likely to be caused by differences expressed at the gametocyte-to-zygote transition. Therefore,
Acknowledgements
I apologize to the authors of relevant publications that I was unable to cite because of space limitations. The valued critique by four anonymous reviewers contributed greatly to this article. This work was supported by a grant from the National Institutes of Health (AI48813). This article is dedicated to the memory of Dr Mohammed Shahabuddin.
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