Muscles or testes? Comparative evidence for sexual competition among dioecious blood parasites (Schistosomatidae) of vertebrates.

Schistosomes, which live as parasitic adults in the blood vessels of mammals, birds and crocodiles, are unique among trematodes because they have separate sexes. Several studies have shown that the sex ratio is often biased towards males. Sexual dimorphism can be very important in several genera (Schistosoma, Heterobilharzia, Schistosomatium), as larger males grip smaller females in a gynecophoric canal. But not all schistomatid species have developed a gynecophoric canal. It is also striking that the number of testes varies widely, from a small number of testes reported (2-7) to a very high number (> 500). We tested the hypothesis of trade-off investment by males: muscle (as estimated by the length of the gynecophoric canal) in order to sequester one or a few females, or testes in order to inseminate numerous females. We used recent comparative methods, which need phylogenetic information of the analysed species. We employed a morphological cladistic analysis of the Schistosomatidae and a construction of a phylogenetic supertree of Schistosoma based on available molecular information. Our phylogenetic analysis supports previous hypotheses on the origin and diversification of the schistosomes. The family seems to have originated as parasites of crocodiles (or possibly other related poikilotherms) and to have secondarily evolved within the Aves and then mammals. Our phylogenetic analyses show that (1) the possession of a gynecophoric canal is a plesiomorphic character, and several reductions of this character have occurred during the diversification of the Schistosomatidae; (2) a small number of testes is a plesiomorphic stage, and an increase of testes number has occurred several times. Finally, our comparative analysis suggests that there is a trade-off between investment in muscle or in number of testes (other variables being controlled for). Male competition for access to females seems to follow two ways: investment in testes in order to fertilize a high number of females or investment in muscle in order to hold and sequester one (Schistosoma) or a few females (Heterobilharzia). We show the existence of the trade-off between muscles and testes in connection with a male biased sex ratio. The development of dioecy cannot explain the trade-off between muscles and testes, which instead appears to be a result of sexual selection possibly driven by the male biased sex ratio.