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How does natural selection act on malaria sex ratios?
Members of the protozoan phylum Apicomplexa, which include the causative agents of some of the most serious diseases of humans and livestock, have dimorphic sexual stages. They have sex ratios which are frequently female biased, and highly diverse. Sex allocation theory has been highly successive at explaining quantitative variation in sex ratios in multicelled organisms. We are using it to understand sex ratio variation in malaria parasites and related protozoa.
There are at least four reasons for bothering.
First, and not least, Apicomplexan sex ratios are often highly variable, both within and between hosts. Explaining the maintenance of diversity in a trait as closely related to fitness as is sex ratio is of interest in its own right.
Second, the population structure of parasitic protoza has proved hugely controversial, particularly in the context of Plasmodium, where population structures from effective panmixia to full clonality have been proposed. The population genetic structure of these parasites is likely to affect the evolution of drug resistance and virulence, and is also relevant to disease diagnosis and the development and assessment of chemo- and immuno-therapy. The key issue is the frequency of self fertilisation. Selfing rates can be measured directly and indirectly by population and molecular genetic methods. These approaches are expensive and the inferences drawn have frequently proved controversial. We believe that sex allocation theory may provide a rapid and cheap method for inferring selfing rates in these populations; we might even go so far as to argue that might be more accurate (Nee et al. 2002).
Third, much of what has been optimisitically called Darwinian Medicine involves the application of adaptationist arguments to infectious diseases, particularly in the context of disease severity. Optimality arguments typically assume population dynamic equilibria. These are not an obvious feature of many medically relevant diseases where epidemic or unstable dynamics are both expected and frequently observed. If infectious diseases do not successfully yield to sex allocation theory, one of the most successful applications of adaptationist thinking, then there is little reason to think that adaptationist arguments concerning more complex phenotypes like virulence will progress much beyond just so stories.
More particularly, the evolution of parasite sex ratio and virulence both depend on the number of parasite clones per host, and they can be modelled in the same way. Thus, not only does analysis of sex ratios in these parasites allow testing of models mathematically analogous with virulence models, but optimal sex ratio and optimal virulence should be positively related. It may therefore be possible to explain and predict virulence evolution using sex allocation.
Fourth, in light of the outstanding success of sex allocation models across a range of biological systems, failure of an apparently appropriate model in a particular context probably points to flaws in our understanding of the basic natural history of the system. For instance, local mate competition theory (Hamilton 1967) successfully predicts sex ratios across populations of Leucocytozoon spp. in birds but it conspicuously fails to do so across populations of a related genus, Haemoproteus, also in birds (Read et al. 1995, Shutler et al. 1995). This immediately focusses attention on details of breeding systems, vectors, or the epidemiology of Haemoproteus species which may not be, as assumed, simply analogous to species in better known taxa such as Plasmodium (Shutler & Read 1998). Formally, of course, failure of apparently appropriate models might point to a failure of theory rather than misunderstandings of the natural history. As things stand, we see no reason to suppose that the study of apicomplexan sex ratios will require a radical expansion of sex allocation theory, but we would be delighted to be wrong.
Issues currently under investigation: (proximate) environmental determinants of sex ratio, including EPO and relatedness within an infection, sex ratios at very low gametocyte densities (where fertility insurance should favour sex ratios closer to unity), and the effects of sex ratio on transmission success.
Group members involved: Sarah Reece
Collaborators: Stu West