This review examines the sexual development of Plasmodium spp. particularly relating the ultrastructural organization of their cells to the limited, though rapidly expanding, body of metabolic and biochemical studies. Thus it is hoped the article may provide a useful background of information for those undertaking studies on the sexual parasites with the objective of developing methods for the immunological and chemo-therapeutic control of malaria transmission. These objectives, however, should not dominate our clear recognition that the three phases of sexual development, gametocytogenesis, gametogenesis and fertilization contain within them examples of control and assembly of organelles without peer amongst eukaryotic cells.

The commonly held view that the kinetoplastida, and in particular trypanosomes, are asexual is largely derived from the principle that an organism is asexual until proved sexual. If the basis for this view is examined in detail, it largely arises from the lack of morphologically distinguishable gametes, the difficulties encountered in visualizing chromosomes and a few experiments, using drug-resistant stocks, in which no recombination between stocks could be demonstrated. While it is clear that these organisms are able to reproduce asexually, the existence of a sexual cycle was, until recently, an entirely open question. The early work strongly suggests that any sexual process (in the species examined extensively at the morphological level) does not involve classical well-differentiated gametes and so must involve fusion of morphologically very similar cells. These findings taken together with the inability to visualize chromosomes and thereby identify meiosis, mean that classical methods are unable to detect any sexual process even if it did occur. This review examines the evidence provided by the experimental approaches which have been applied recently to the question of kinetoplastid sexuality. These approaches include isoenzyme studies and the analysis of possible genetic exchange by the use of selective markers (e.g. drug resistance). The results which these techniques have produced make it clear that the kinetoplastid protozoans cannot be regarded as a totally asexual group of organisms.

Pentastomids are arthropod parasites which attain maturity in the respiratory tracts of vertebrates. All pentastomids exhibit an obvious sexual dimorphism in that fully mature females are invariably much bigger than males. Unusually though, copulation, which happens only once in the lifetime of females, occurs when both sexes are approximately the same size and the uterus of the female is undeveloped. This is because sperm is stored in spermathecae which, being positioned at the junction of the oviduct and uterus, become more remote from the vagina as the uterus elongates during development. The provision of spermathecae for sperm storage allows oocytes, shed continuously from the ovary, to be fertilized from time to time. What renders this process quite remarkable, and possibly unique, is the extreme length of the patent period. In one species this can extend up to an estimated 10 years and is associated with an egg production of about 106 eggs/female/year. Spermathecal structure provides some clues as to how prolonged sperm storage and the continuous fertilization of oocytes is accomplished. The upper region of the access duct is a narrow, chitinized tube which tapers to as little as 3 μm diameter at the point of entry into the spermatheca. The chitinous (?) lining of the spermatheca is relatively impermeable and apparently functions to totally isolate sperm from external influences: stored sperm are arranged in bundles and whorls and remain totally quiescent and inactive during the storage period. The entire spermatheca is invested by muscle fibres, the contraction of which will express small numbers of sperms through the narrow access duct. These are then reactivated by secretions from the female reproductive tract: the extreme narrowness of the spermathecal duct provides the fine adjustment of the system. The narrowness of the duct also creates problems during the process of insemination, since sperm discharged directly into the female reproductive tract would be unlikely to find the spermatheca through such a structure. Accordingly, the male cirrus is much modified to directly penetrate the spermathecal duct during copulation. Sperms, stored in the male seminal vesicle, are apparently activated prior to sperm transfer, and swim along the cirrus to be guided directly into the spermathecal lumen. Some unusual variations on the normal pentastomid life-cycle are discussed.

The high energy costs of egg-shell production in many helminths suggests that this structure plays an important role in their biology. The mechanical and chemical resistance of the egg-shell and the barrier it provides to the entry and loss of material are important in the survival of the free-living stages within the egg. The presence of egg filaments may increase the availability of infective stages and the operculum may be important in the infective process.

Previous studies on the spermatogenesis and oogenesis of digeneans, monogeneans and cestodes are reviewed, including those in which isotopic labelling techniques have been utilized in order to determine the temporal duration of spermatogenic development stages. Similar labelling experiments have also provided information on the development and movement of oocytes in the female reproductive tract as well as indicating patterns of cell division and development in vitelline glands. The literature relating to the inseminative behaviour of parasitic platyhelminths is considered from a number of viewpoints including the patterns of cross-and self-insemination that occur in hermaphroditic digeneans, the mating behaviour of dioecious schistosomes, spermatophore production and insemination among monogeneans and the inseminative behaviour of polyzoic cestodes. The implications of selfing among parasitic platyhelminths are considered with respect to possible genetically deleterious consequences. In addition, consideration is given to the mechanisms underlying the fact that some species require cross-insemination or at least the presence of another worm in order to undergo normal growth and sexual development. Finally, experimental studies are reviewed which shed light on the strength of the barriers against hybridization that exist between well-defined species of parasitic platyhelminths.

Among flatworms with parasitic and commensal modes of existence, parthenogenesis and asexual multiplication appear to be largely confined to the Digenea and Cestoda, the only parasitic platyhelminths that routinely utilize indirect life-cycles. Parthenogenesis is apparently restricted to a minority of adult digeneans and cestodes inhabiting their final hosts, and a survey is made of the particular modes of parthenogenesis (i.e. apomictic, automictic and generative) which are employed by such adults. Asexual (amictic) multiplication, in the form of fissioning, is demonstrated by young adults of the cyclophyllidean cestode, Mesoces-toides corti, but is otherwise not exhibited by adult cestodes or digeneans, other than in the perplexing phenomenon of proglottid formation in polyzoic tapeworms. Secondary multiplication is of ubiquitous occurrence in digenean life-cycles in the form of the proliferation which takes place within sporocysts and rediae (germinal sacs) located in the first intermediate host. The controversy concerning the nature of this multiplication is reconsidered in the context of recent findings which have centred on cellular aspects. On the basis of present evidence germinal sac multiplication should be regarded as an asexual rather than a parthen-ogenetic process. The cestode asexual multiplication which occurs in intermediate hosts is a function of the metacestode stage of development. Metacestode proliferation is only known from about 20 species and 6 families of polyzoic cestodes with approximately half the described instances occurring in the family Taeniidae. The organization of these proliferative metacestodes, findings concerning their totipotent stem cells and the ontogeny of buds and new scolices are all reviewed. Finally, the capacity for population expansion of multiplicative larval digeneans and metacestodes are compared, while the ecological roles and the genetical consequences of both parthenogenesis and amictic multiplication in the two taxa are also examined.

The encapsulated embryos of platyhelminths may be retained and complete their development in utero in a range of circumstances. However, hatching within the parent (the criterion of ovoviviparity) is relatively rare and larvae generally emerge only after deposition. Viviparity is characterized by the nutritional dependency of the unencapsulated larva upon the parent, but in several cases larvae retained within a shell also receive parental nutrients during intra-uterine development. Uptake of exogenous nutrients via shell pores occurs in Schistosoma mansoni but the eggs, which gain all the advantages of intra-uterine retention, are supported by host nutrients.

Intra-uterine larval development avoids the hazards of development in the external environment and eliminates the time delay between oviposition and infection. Deposition of immediately infective offspring may be concentrated in time and space to exploit periods of host vulnerability. The control and precision of transmission is illustrated by examples in which the opportunity for invasion is restricted because of either host behaviour or environmental instability. This strategy has been an important factor in the evolution of polystomatid monogeneans, and its effectiveness is demonstrated by comparison of the life-cycles of Polystoma integerrimum and Pseudodiplorchis americanus. Ovoviviparity also increases reproductive potential in some polystomatids by extending the period of multiplication and by increasing established populations through internal re-infection. In Eupolystoma alluaudi, the capacity for ovoviviparity is programmed into larval development and this regulates population growth within individual hosts.

Parasites are more fecund than free-living relatives. The traditional explanation of this is that parasites have to compensate for massive mortality in the transmission phase of their life cycles, but there are neo-Darwinian problems with this interpretation. Similarly, parasites invest more resources in reproduction than free-living relatives but often live longer as adults, and yet negative correlations are expected between fecundity and longevity. These patterns and paradoxes are discussed within the context of a general life-cycle theory. The theory is also used to address questions concerning the influence of age-specific mortality on life-cycle patterns, the trade-off between gamete size and numbers, and the relative merits of gametic and non-gametic reproduction. Wherever possible, the theory is related to facts about parasites.