strategy may be appropriate. To what extent sex determination can
be adaptive when faced with such uncertainty will be addressed with
reference to one such complex but well-studied system – malaria and
related parasites in their vertebrate hosts.Malaria and related parasites – a worked example
Malaria parasites belong to the haemosporidian apicomplexan proto-
zoans, which share a similar life cycle (Box 10.1), proliferating asexually
within their vertebrate host and transmitting via an insect vector. At
some point during infection, a proportion of the parasites switches from
asexual- to sexual-stage production. In addition to commitment to sexual
differentiation (gametocytogenesis), malaria parasites determine the sex
of their gametocytes (male or female). During its entire cycle in the
vertebrate host,Plasmodiumis haploid and there are no sex chromo-
somes. Each clone is capable of self-fertilization, producing both male
and female gametocytes, i.e. it is a simultaneous hermaphrodite.In vitro
culture ofPlasmodium falciparumhas shown that the proportion of male
and female gametocytes is fixed, clone-specific and therefore genetically
determined (Ranford-Cartwrightet al., 1993). How sex is determined is
unknown, but it appears, at least forP. falciparum, to occur at the moment208 R.E.L. Paul
Box 10.1. Malaria-parasite life cycle (Carter and Graves, 1988; Sindenetal.,
1996)At blood-feeding, an infected mosquito injects parasite sporozoite stages, which
invade vertebrate host cells. These sporozoites undergo asexual proliferation in
their host cells, producing many hundreds of thousands of merozoite-stage para-
sites. These merozoites invade erythrocytes, where they grow, divide asexually to
produce further merozoites and burst out of the cell to invade further erythrocytes,
a cycle occurring every 24, 36 or 48 h, according to thePlasmodiumspecies. At
some point during the course of the infection, most notably when such asexual
proliferation is slowed, the merozoite stages grow but do not divide, and thus pro-
duce the sexual stages, the gametocytes, which are gamete precursors. Trans-
mission from the vertebrate host to the mosquito vector is mediated solely by these
sexual stages of the parasite, which are distinguishable as males and females.
When taken up in the blood meal by another female mosquito, these gametocytes
transform into gametes: each male gametocyte undergoes exflagellation, by which
process up to eight male gametes are produced; each female gametocyte
produces only one female gamete. Such gametogenesis occurs within 10–15 min
following uptake in the blood meal, and within 30 min the male must actively swim
to find and fertilize the female gamete. The subsequent zygote transforms into a
mobile ookinete, which penetrates the mosquito midgut, where it encysts. Eight to
15 days later (depending on thePlasmodiumspecies), this mature oocyst bursts,
releasing several thousand sporozoites, which invade the salivary glands of the
mosquito and are injected into the vertebrate host during its next blood meal.