male are only able to fertilize the gamete from their paired female. Syzygy
therefore removes the factors favouring female-biased sex ratios under
LMC: increasing female number will not reduce competition among male
gametes from the same gametocyte and will not allow an increase in
fertilization success by a single male gametocyte. As predicted, species
with syzygy (adelorin species, including the hepatozoans) tended to have
an even sex ratio (Westet al., 2000).
There is therefore some field evidence that LMC shapes malaria-
parasite sex determination and that optimal sex ratios will vary according
to the parasite population structure and hence the transmission intensity
of the parasite. However, a cross-sectional study found that, although the
modal sex ratio was female-biased, transmission success increased with
sex ratio, i.e. the sex ratio that maximized mosquito infection rates was
neither the most common nor that expected under LMC (Robertet al.,
1996). This apparent paradox may simply reflect more complex sex-
allocation strategies: in contrast toin vitrocultures, thePlasmodiumsex
ratioin vivois not fixed but can vary during the course of infection. It has
been known since the mid-1900s (James, 1931; Shute and Maryon, 1951)
that the gametocyte sex ratio could vary quite dramatically during the
course of a single infection, although with little clear significance for
transmission success. Of what adaptive value, if any, therefore is such a
fluctuating sex ratio? There is considerable, albeit anecdotal, evidence
that males are a limiting factor. Boyd (1949) first noticed the importance
of the number of male gametocytes and suggested that the number of
males rather than females determine infection success. In addition, a
comparison of clones from a single isolate adapted toin vitroculture
showed that the less female-biased sex-ratio clones were more infectious
to mosquitoes (Burkot et al., 1984). Furthermore, the importance of
insurance males was suggested as an explanation for the more even sex
ratios inHaemoproteus, where small blood-meal size would decrease the
probability of taking up a male. In malaria parasites, although LMC may
operate, the need for insurance males may alter the optimal sex ratio, but
does so only under specific conditions – i.e. when the habitat becomes
deleterious for reproduction and insurance males are beneficial. Such
flexibility in sex allocation would require the ability to respond to the
environment and facultatively alter sex ratio accordingly. Two possible,
but not exclusive, explanations are therefore considered: (i)Plasmodium
can alter its sex ratio facultatively according to the number of coinfecting
clones (facultative LMC); and (ii) variable host quality jeopardizes
reproduction and selects for insurance males.Facultative LMC
One interpretation of these fluctuating sex ratios inPlasmodiumhas
been proposed from longitudinal gametocyte sex-ratio data in lizard
populations (Pickeringet al., 2000). Here, the sex ratio was found to beParasite Sex Determination 211