Sex Loss in Monogonont Rotifers

Abstract

Monogonont rotifers are small, aquatic invertebrates capable of asexual and sexual reproduction. Sexual reproduction is required to produce diapausing eggs, which are able to survive adverse periods that typically occur every year. Their cyclically parthenogenetic life-cycle is believed to retain the advantages of recombination while minimizing the cost of sex. However, this life cycle is also thought to be unstable due to periodic loss of sexual reproduction by directional selection. Explaining the evolutionary dynamics of the monogonont rotifer life cycle is important for understanding how cyclical parthenogenesis is maintained, and for comparing monogononts with their close relatives, the bdelloid rotifers, which are ancient obligate asexuals. Our analysis clarifies that the cost of sex in monogononts is two-fold when compared to an obligate asexual lineage on an annual time-scale. However, when compared to an obligate sexual, cyclical parthenogens avoid the cost of sex in every parthenogenetic generation. In monogonont rotifers, where sexual reproduction is triggered by crowding, reproducible loss of sex has been reported in laboratory experiments. The mechanistic hypothesis is that some obligate asexual clones arise by spontaneous mutation, and they fail to respond to the sex triggering chemical signals produced by conspecifics. Hence, in these clones, asexual females never produce sexual daughters. Using a simple model, we show that as a result of this association of sex with dormancy, sex loss results in a huge short-term advantage, because sexual females only produce males or diapausing eggs, and do not contribute to current population growth. However, the requirement of sex for dormancy should result in a mid-term selection pressure to retain sex. It is this mid-term pressure that stabilizes cyclical parthenogenesis and allows it to persist. From this analysis, the periodic occurrence of obligate asexuals is predicted in monogonont rotifer populations, especially those with infrequent adverse periods.