Female Polymorphism and Sexual Reproduction in the Rotifer Asplanchna: Evolution of Their Relationship and Control by Dietary Tocopherol

The adaptive significance of the control of sexual reproduction in heterogonic life cycles by different types of environmental factors is considered. In several of the more carnivorous species of the rotifer Asplanchna, the incidence of sexuality is directly associated with a nongenetic female polymorphism controlled by dietary tocopherol (vitamin E). Knowledge of this relationship is reviewed, and two theories attempting to explain how such a system might have evolved are evaluated. The hypothesis that tocopherol is required for male fertility and thus serves as an adaptive signal for male production is untenable. The following alternative hypothesis and its corollaries are favored. The initial response to tocopherol was a general growth increase which permitted Asplanchna to more easily ingest larger, and possibly more nutritious, herbivorous prey. The tocopherol molecule is an adaptive cue for this growth response for several reasons: (1) since it is synthesized only by photosynthetic organisms and readily assimilated by herbivores, its ingestion by the predatory Asplanchna indicates the availability of herbivorous rotifer and crustacean prey; (2) since it is readily assimilated by Asplanchna and efficiently transmitted without degradation to its embryos, it is in a position to exert a well-buffered, inductive effect over several generations during embryogenesis and postnatal development; (3) it can itself promote growth in Asplanchna through increased cell enlargement, cell division, and possibly DNA endoreduplication. Mictic-female production then became associated with the growth response because the latter indicated conditions favorable for a period of sexual reproduction-a nutritious diet of herbivorous zooplankton, which would be associated with a high or increasing population density suitable for facilitating contacts between males and mictic females and which would permit the formation of energy-rich resting eggs. Body-wall outgrowths, which reduced cannibalism by the large individuals, then became associated with the growth response to tocopherol. Two tocopherol-dependent, female morphotypes evolved in some species. The larger, campanulate morphotype was adapted for ingestion of very large prey and, in one species, for exclusively parthenogenetic reproduction. The well-protected cruciform morphotype, with prominent body-wall outgrowths, was adapted for ensuring sexual reproduction and avoiding capture by cannibalistic conspecifics. Four closely related species of Asplanchna respond very differently to tocopherol and provide some evidence for a proposed scheme describing the evolution of tocopherol-dependent morphotypes. Asplanchna girodi does not respond to tocopherol and has monomorphic females. A. brightwelli, A. intermedia, and A. sieboldi have increasingly more complex and extensive responses to tocopherol. The selective pressures resulting in this progression seem to be related to increasing availabilities of zooplankton prey. Growth responses to tocopherol evolved only in those species which do not depend on the direct utilization of relatively small tocopherol-rich algae and which can ingest copious quantities of zooplankton prey needed for sustaining populations of large individuals.