Controlling and coordinating development in vector-transmitted parasites

Abstract

Vector-borne parasites cause major human diseases of the developing world, including malaria, human African trypanosomiasis, Chagas disease, leishmaniasis, filariasis, and schistosomiasis. Although the life cycles of these parasites were defined over 100 years ago, the strategies they use to optimize their successful transmission are only now being understood in molecular terms. Parasites are now known to monitor their environment in both their host and vector and in response to other parasites. This allows them to adapt their developmental cycles and to counteract any unfavorable conditions they encounter. Here, I review the interactions that parasites engage in with their hosts and vectors to maximize their survival and spread.

Fig. 1. The global distribution of vector-borne human diseases.

The individual parasites and their vectors are indicated in the table, as are the diseases they cause and their main geographical distributions.

Fig. 2. Factors that influence the development of parasites as they pass through their mammalian host or vector.

In each case, host- and parasite-moderated conditions can determine the developmental fate of the parasite. During transmission between the mammalian host and the vector and during establishment in the vector, there is often a significant amount of parasite death.

Fig. 3. Routes of transmission of different parasite groups through an arthropod vector.

Plasmodium male and female gametocytes fuse to generate a zygote, which then matures to an ookinete that penetrates the gut lining of the mosquito vector. This develops into an oocyst, within which sporozoites develop. Sporozoites are released and migrate to the mosquito salivary gland, where they are infective to a mammalian host when the mosquito seeks a blood meal. For helminths, microfilariae are ingested during blood feeding by mosquitoes (Wurcheraria and Brugia) or blackflies (Onchocerca). The worms then migrate through the hemocoel, eventually reaching the proboscis and salivary glands, where they can be transmitted to a new host. For kinetoplastid parasites, ingested nonproliferative transmissible forms develop into proliferative forms that establish in the alimentary canal of their vector. For T. brucei, the parasites then migrate via the proventriculum of the tsetse fly to the salivary glands, where they attach and multiply as epimastigote forms before forming infective metacyclic forms. For T. cruzi and Leishmania, the parasites multiply in the gut of the kissing bug and sandfly vectors, respectively, before maturing into infective forms (trypomastigote forms in T. cruzi or promastigote metacyclic forms in Leishmania) in either the hind gut or pharyngeal valve, respectively. T. cruzi are transmitted by expulsion during bug defecation, parasites being rubbed into the bite wound. The challenges faced by the parasite within its invertebrate vector are indicated above the diagram.