Evolution of mating tactics and reproductive strategies in protozoan parasites

The Phylum Apicomplexa (Protozoa) includes some of the most serious pathogens of livestock and humans. Despite extensive funding efforts, we understand remarkably little about the strategies they have evolved in order to maximise their reproductive success. These parasites, including malaria (Plasmodium) parasites, must undergo a round of sexual reproduction inside their vectors in order to transmit to new hosts. Once inside a vector's blood meal, sexual stages rapidly differentiate into gametes and fertilisation between male and female gametes occurs. However, a blood meal is a very harsh environment to be mating in, as blood is rapidly cooling and clotting. This also exposes gametes to both their host's immune factors and their vector's digestive chemicals. Consequently, male sexual stages have a maximum of 20 minutes to exit their red blood cells, differentiate into gametes and find females to fertilise. Furthermore, unlike most other male animals, male malaria parasites can only produce a maximum of eight gametes. This makes the mating system of malaria parasites very novel, yet, there is remarkably little data available and important questions remain unanswered. This proposal will discover how mating between malaria parasites is influenced by host immune factors, ask whether males randomly search for females or can home in on their location, and will investigate how co infecting species of malaria parasite maintian their species identity. A greater understanding of how and why organisms adopt the strategies we observe provides fundamental insights into the process of adaptation, as well as having valuable practical applications in areas ranging from medical science to conservation. Given the medical and economic importance of malaria parasites and the drive to develop transmission blocking vaccines and intervention strategies, understanding this process from an evolutionary and ecological perspective is of crucial importance.

Achievements, Findings & Significance
The work proceeded as planned and six papers have been published (see dissemination section in JeS form) and another two (detailed at the end) are in prep.
(1) Social factors proved to be extremely interesting and this project is being further developed in a PhD project. Experiments revealed that contrary to conventional wisdom, different species can mate and form zygotes infective to mosquitoes. However, this only occurs when genes for certain surface proteins are missing, indicating that these molecules act as species-labels. These findings are important for our understanding of parasite transmission, speciation and have broader implications (e.g. transfer of drug resistance genes).
(2) Experiments revealed that parasites do not facultatively alter sex allocation within infections in response to the general immune status of their host. But specific immune factors do influence reproductive success; TNF-a reduces the survival of females and/or zygotes but not males and nitric oxide only reduces the fertility of males. These results are being extended to within- infection manipulations and the broader implications for sex allocation.
Future Outlook
This grant and funding my postdoctoral fellowship (NE/B501755/1) have provided the foundtations for me to develop this research in several directions and build a long term research project. In particular, I have atrracted a PhD student to develop the mating and hybridisation project and am using a Wellcome Trust career development fellowship to develop the immune environment results.
Papers
Drew D.R., Reece S.E. (2007) Development of reverse transcription PCR techniques to analyse the density and sex ratio of gametocytes in genetically diverse Plasmodium chabaudi infections. Molecular and Biochemical Parasitology 156(2):199-209
Reece S.E., Innocent T.M., & West S.A. (2007) Lethal combat in the parasitoid, Melittobia acasta: are size and competitive environment important? Animal Behaviour 74: 1163-1169
Innocent T.M, West S.A. & Reece S.E. (2007) Lethal combat and sex ratio evolution in a parasitoid wasp. Behavioural Ecology 8(4): 709-715
Augustijn K.D, Kleemann R., Thompson J., Kooistra T., Crawford C.E., Reece S.E., Pain A., Siebum A.H.G., Janse C.J. & Waters A.P. (2007) Functional characterization of the Plasmodium homologue of Macrophage Migration Inhibitory Factor (MIF). Infection & Immunity 75(3): 1116-1128
Shuker D.M., Reece S.E., Lee A., Graham A., Duncan A.B., & West S.A. (2007) Information use in space and time: sex allocation behaviour in the parasitoid wasp Nasonia vitripennis. Animal Behaviour 73(6): 971-977
Culleton R.L., Cheeseman S., Martinelli A., Byrne J., Steven L., Reece S.E., Carter R. (2006) Strain-specific immunity to the pre-erythrocytic stages of Plasmodium chabaudi. Proceedings 11th International Congress of Parasitology. 2006: 319-323