Evolution of asexuality in experimental rotifer populations

Most multicellular organisms reproduce sexually, despite high costs associated with this reproductive mode (i.e., costs of males, costs of meiosis, costs associated with finding mates or mating itself). In the last three decades this "paradox of sex" has received considerable attention of both theoreticians and empiricists. Nonetheless, a single and universal explanation for the ubiquity of sex has remained elusive. In particular, explanations on the "paradox of sex" are challenged by the existence of organisms that frequently give rise to obligate asexual lineages. Such organisms should constantly face the danger of being displaced by their asexual variants. Hence, what holds these newly arising asexuals at bay? In this project, the monogonont rotifer Brachionus calyciflorus shall be used as a model system to address this question. The Brachionus system is distinct from most previously used animal models, because it allows an experimental approach: Rotifers have generation times of a few days only, they reproduce fast, and transitions to obligate asexuality can occur on time scales of weeks. In addition, rotifers are small and populations of thousands can be easily kept in laboratory, which allows studying evolutionary changes on the population level. The proposed work addresses three main questions: (i) What is the general mechanism of origin of obligate asexuality in Brachionus? (ii) How fit are asexuals compared to their sexual relatives - under which conditions will they spread/decline? (iii) What is the significance of obligate asexuality in field populations of Brachionus? A variety of methods will be used to answer these questions: lab and field experiments, molecular techniques (DNA barcoding, microsatellites), karyological methods, and automated lab cultures (chemostats). The results are expected to yield new insights into the "paradox of sex", particularly in terms of the factors influencing the success/failure of new asexual lineages. In addition, the expected results will likely contribute to a better understanding of the origin of asexuality in bdelloid rotifers, a sister group of monogonont rotifers that has evolved in the absence of sex for millions of years.

Most multicellular organisms reproduce sexually, despite high costs associated with this reproductive mode (i.e., costs of males, costs of meiosis, costs associated with finding mates or mating itself). In the last three decades this paradox of sex has received considerable attention of both theoreticians and empiricists. Nonetheless, a single and universal explanation for the ubiquity of sex has remained elusive. In particular, explanations on the paradox of sex are challenged by the existence of organisms that frequently give rise to obligate asexual lineages. Such organisms should constantly face the danger of being displaced by their asexual variants. Hence, what holds these newly arising asexuals at bay? In this project, the monogonont rotifer Brachionus calyciflorus was used as a model system to address this question. Normally Brachionus rotifers reproduce by cyclical parthenogenesis (CP), which is an alternation of sexual and asexual reproduction (parthenogenesis), but occasionally obligate parthenogenesis (OP) can arise. Such transitions have been described in laboratory populations, yet until the start of this research project essentially nothing was known about the mechanism of origin. A major result of this research project was the discovery that obligate parthenogenesis in Brachionus was caused by a mutation at a single gene. Mutants carrying two copies of that gene have completely lost their ability to reproduce sexually. OP mutants also showed dwarfism (body size was reduced up to 50%) but they were otherwise very similar to their sexual relatives, e.g. in terms of basic life history characteristics such as survival and reproduction. However, since these OP mutants spared the costs of sex they could competitively displace their sexual relatives within only a few days. This was demonstrated in mathematical models and confirmed by experiments with evolving populations. Populations composed solely of OP mutants differed substantially from populations with sexual reproduction. For example, they exhibited much higher population densities (a higher carrying capacity) and a stronger depletion of their food resources. Furthermore, OP populations were inherently unstable in the long term, both because they exhibited higher fluctuations in population density and because they lacked the resting eggs, which are a major prerequisite for populations to deal with the seasonality of natural habitats. In conclusion, the transition to asexuality in Brachionus appears to be beneficial in short-term but ultimately results in populations that are doomed to extinction. In the future, this experimental system should enable us to probe deeper into the general mechanisms that stabilize sexual reproduction. For instance, the possibility to generate closely related individuals with either sexual or obligate asexual reproductive mode provides a unique experimental tool for studying the benefits of sexual reproduction, and it also should allow pinpointing important molecular mechanisms of sexual and asexual reproduction.