We review methods for studying the adaptive basis of sex allocation in the phylum Apicomplexa, a group of parasitic protozoa that includes the aetiological agents of malaria. It is our contention that analysis of apicomplexan sex ratios is not only interesting in its own right, but may actually provide insights into matters of clinical and epidemiological importance. We begin by justifying that position, and then summarize the natural history of these parasites and the sex ratio expectations that flow from that. Broadly speaking, these expectations are supported, but the evidence is scanty relative to that for many multicelled taxa. In the second half of the chapter, we give an overview of the theoretical and empirical methods available to take this work further. Much remains to be done: many key assumptions are currently little more than acts of faith.
Almost all work on the evolution of sex allocation is motivated by and tested on multicelled organisms. Yet the causative agents of some of the most serious diseases of humans and livestock have anisogamous sexual stages (Figure 15.1). These are all members of the protozoan phylum Apicomplexa, and include the malaria parasites (Plasmodium spp.). Species in other protozoan phyla can also have anisogamous sexual stages (e.g. some dinoflagellates, volvocidians and perhaps some foraminiferans; Lee et al. 1985) but we are unaware of any analysis of sex allocation in micro-organisms other than the Apicomplexa.
Many see research into sex allocation as the jewel in the crown of evolutionary ecology. There is a very rich experimental literature providing qualitative, and in some cases quantitative, support for the predictions of numerous theoretical models. Consequently, it might be argued that future work will primarily be concerned with dotting i's and crossing t's. Given that there are still so many relatively untamed areas in evolutionary biology, we should therefore ask – why bother with more sex-allocation studies? Our aim in this chapter is to address this question (why?), complementing the more methodological (how?) parts of this book. We argue that sex allocation is an excellent model trait for examining general questions in evolutionary biology.
The usefulness of sex allocation
The strength of sex-allocation research arises for both theoretical and empirical reasons. Sex allocation has a direct and potentially large influence on fitness, and the relevant trade-offs are easy to quantify. Consequently, optimality models are able to make clear theoretical predictions in many specified cases. Empirically, sex allocation can be a relatively easy trait to measure. This is especially true in cases where males and females are equally costly to produce, and so we can concern ourselves simply with the sex ratio (defined as proportion males, i.e. males/(males+females)). In this case, all we must do is count the number of male and female offspring that are produced.
We use a detailed case study to identify considerations that are likely to be important in constructing and interpreting tests of the optimality of adaptations. Specifically, we consider the sex ratio responses in natural populations of 15 fig-pollinating wasp species and the predictions of local mate competition theory. The mean sex ratios exhibited by fig wasps show qualitative and often quantitative agreement to a wide range of predictions of these models. However, we also find (1) deviations of mean responses from theoretical optima, (2) variation among individuals in their responses to given situations, and (3) unresolved doubts concerning the parameterization and applicability of the models used to predict optimal brood sex ratios. A fundamental question in interpretation arises: Are we using the theory to test the precision of adaptation, or are we using the responses to test the precision of the models? A partial solution to this problem is offered by the fact that within and across these fig wasp species, the frequency with which any particular situation occurs (i.e., selective regime) can be estimated. Across species, the deviations from the predicted optima are fewest in the situations most frequently encountered by the organisms. Similarly, variance in the responses of individuals is lowest for those situations most commonly encountered. Furthermore, phylogenetic relationships of the wasps have little or no relationship with means, deviations, or variance of their sex ratios, suggesting that these characters evolve very rapidly with respect to speciation and are not correlated with other characters that are themselves closely correlated with phylogenetic relationships.
Fig–pollinating and fig–parasitizing wasps are integral parts of one of the most fascinating plant–insect interactions known. Moreover, studies of these wasps have been instrumental in developing and refining ideas concerning the influence of population structure and inbreeding on shaping the outcome of kin selection. We present data compiled from six studies spanning five continents that relate brood sex ratios with foundress number in 24 pollinator species. All predictions of local mate competition (LMC) and inbreeding theory are at least qualitatively supported. Additionally, the sex ratios produced by single foundresses of any given species appear to be influenced by brood size and the frequency of multiple foundress broods in that species. We then consider the assumptions underlying the testing of the specific LMC model and consider the relative merits of observational and experimental tests of the theory. Furthermore, we discuss the existing studies of the parasitic wasp species that have addressed the unusual morphological and behavioral polymorphisms for flightlessness and lethal combat that are found in the males of these species. These differences appear to be influenced by the parasites' population structure and density, although other factors are also implicated. Finally, we compare the nature of the support for LMC theory from fig–pollinating wasps with that from the parasitoid wasp Nasonia vitripennis, and suggest future lines of research.
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