Sex ratios are important for transmission
Evolutionary theory predicts that malaria parasites produce the most appropriate number of gametocytes, in the most appropriate sex ratio, to maximise fertilisation (reproductive) success in their vectors. There is widely held belief that the number of gametocytes present in blood meals determines fertilization success, so the sex ratio of gametocytes is rarely considered. However, we have recently shown that sex ratio is an important fitness-determining trait. By using genetically modified P. berghei lines in which either a gene determining male or female fertility have been knocked out, and mixing these lines in different ratios we created mating groups with different sex ratios. This experiment revealed that mating groups with slightly female biased sex ratios had the highest fertilisation success and so extreme sex ratios are selected against (stabilizing selection). More generally, this is first published experimental demonstration of how fitness varies over the range of sex ratios possible (i.e. from 0 - 100% males).
Sex ratios are adjusted according to the inbreeding rate
Sex ratios in malaria parasites are generally female-biased and evolutionary theory predicts that sex ratios reflect the inbreeding rate. As gametocytes taken up in a blood meal reflect the genetic composition of their host's infection, inbreeding occurs if mating groups consist of gametocytes from 1 or small number of genotypes, and outbreeding can occur when multiple genotypes are represented. Female-biased sex ratios are expected when inbreeding occurs because this represents the most efficient allocation of resources to maximize the fertilization success of mating groups. Because each male can fertilise more than one female, a female-biased sex ratio reduces competition for mates between related males and maximises the number of females available to be fertilised. In contrast, when infections are composed of several genotypes the greatest fitness returns come from increasing investment in male gametocytes. In this situation, because each male can mate with several females and unrelated females belonging to other genotypes are present, a genotype that produces more males will have the greatest genetic representation in the next generation.
This is "Hamilton's Local Mate Competition" (LMC) theory and it has been particularly successful in explaining why female-biased sex ratios are favoured in spatially structured populations for a variety of taxa, from plants to insects to snakes. The strongest support for this theory in other taxa has come from experimental tests showing that individuals can evaluate the likely inbreeding rate their offspring will experience and adjust their sex ratio accordingly. Our recently developed molecular assays that are both genotype- and sex-specific have enabled us to conduct analogous experiments in malaria parasites. These experiments have revealed that, whilst they are in their hosts, P. chabaudi genotypes can evaluate the inbreeding rate they will experience in their vectors and adjust their gametocyte sex ratio accordingly.
Success in explaining malaria sex ratios is largely due to the extensive theoretical and empirical attention this trait has received in metazoan taxa. In fact, the allocation of resources to male and female offspring is one of the most well understood topics in evolutionary biology. In many cases, simple theory can successfully predict when, why and by how much organisms should adjust their offspring sex ratio in response to changes in their environment.
However, whilst Hamilton's Local Mate Competition theory explains why malaria sex ratios are usually female biased, it does not explain why sex ratios vary throughout infections in which the inbreeding rate does not change. For more information on why parasite reproductive decisions vary throughout infections see Plasticity In Reproductive Decisions.