Effect of gametocyte sex ratio on infectivity of Plasmodium falciparum to Anopheles gambiae

Abstract

Insectary-reared Anopheles gambiae were experimentally fed with the blood of 90 naturally infected human volunteers carrying gametocytes of Plasmodium falciparum. At least one mosquito was successfully infected in 74% of experiments. The probability that a gametocyte carrier was infective, the probability that a mos quito became infected, and the number of oocysts harboured were related to gametocyte density. The mean oroportion of male gametocytes was 0*217 (i.e., 3-6 females for every male). Sex ratios differed significantly between gametocyte carriers. Variation in sex ratio was not related to the probability that a gametocyte car rier was infective. Among infective people whose sex ratio estimates were based on a reasonable number of gametocytes, sex ratio significantly predicted the proportion of infected mosquitoes and mean oocyst load, with infectivity rising as the proportion of male gametocytes increased towards 50%. There was no indica tion that infectivity reached a peak at some intermediate sex ratio, as would be expected if random mating of gametes was the primary determinant of fertilization success. These results raise 2 interesting questions: why should higher sex ratios be more infective, and why is the observed population sex ratio lower than that which produces the greatest infectivity?

Plasmodium falciparum gametocyte carriage, sex ratios and asexual parasite rates in Nigerian children before and after a treatment protocol policy change instituting the use of artemisinin-based combination therapies

“…In keeping with the fact that Plasmodium species sex ratios are often female biased (Robert et al 1996, Pickering et al 2000, Reece et al 2008, the gametocyte sex ratio in our cohort of children was also female biased and differed little over a 10-year period. The gametocyte sex ratio of 0.20-0.21 suggests, theoretically, that this is the maximum degree of female bias expected if the average number of viable gametes released after exflagellation by one male gametocyte was four (Read et al 1992.…”

“…The gametocyte sex ratio of 0.20-0.21 suggests, theoretically, that this is the maximum degree of female bias expected if the average number of viable gametes released after exflagellation by one male gametocyte was four (Read et al 1992. The population sex ratio in this endemic area is similar to that reported in neighbouring Cameroon [0.217 (Robert et al 1996)], but it is lower than the 0.346 reported in Senegal (Robert et al 2003). In this endemic area clone multiplicity in P. falciparum infections is approximately three-four (Happi et al 2003(Happi et al , 2004(Happi et al , 2006) and this appears to have changed little over the years (Happi et al 2003(Happi et al , 2004(Happi et al , 2006.…”

“…Using this approach, AL effectively shortened the duration of male gametocyte carriage in individual patients following treatment. If at low gametocytaemia, a male-biased sex ratio is crucial to malaria transmission (Robert et al 1996, Mitri et al 2009, Ouédraogo et al 2009), then AL can be expected to reduce the duration of exposure to potentially successful mosquito infectivity following a blood meal by shortening the duration of male gametocyte carriage compared to CQ. Could this effect produced by AL or other ACTs significantly influence malaria transmission in this endemic area?…”

“…Mosquito infectivity after a human blood meal and the subsequent transmission is thought to be dependent on gametocyte density (Tchuinkam et al 1993, Robert et al 1996, Ouédraogo et al 2009) and may be influenced by the gametocyte sex ratios (GSR) in the blood meal (Robert et al 1996, Mitri et al 2009). It has been shown that the proportion of infected mosquitoes and the mean oocyst load increased as sex ratio in the infected human blood meals increased towards 0.5 (Robert et al 1996). In cultured gametocytes, increasing the male sex ratio increased the mosquito infectivity rate at low levels of gametocyte density, whereas there was a reduced infectivity rate at higher levels of gametocyte density (Mitri et al 2009).…”

Some features of primary and recrudescent amodiaquine-resistant Plasmodium falciparum infections in Nigerian children

“…In addition, patients with recrudescent infections were matched for age and gender with patients who had a sensitive response to AQ. Gametocyte sex was determined as described by Carter and Graves (1988) and Robert et al (1996). Gametocyte sex ratio was defined as the proportion of gametocytes that were male (Pickering et al 2000).…”