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Bdelloid rotifers are the most common and abundant group of animals that …

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- Stress and fitness in parthenogens: is dormancy a key feature for bdelloid rotifers?

Nearly all kinds of eukaryotic organisms reproduce sexually by joining the two processes of meiosis and karyogamy: genes from two parents are combined and produce genetically different organisms. A few scattered groups of organisms are able to produce by mitosis, rather than meiosis, female gametes which will develop into offspring that are genetically identical to their mothers. This process is called parthenogenesis and provides faithful replication of the genome, barring mutation, and high reproductive efficiency. Although parthenogens should have a reproductive advantage over their sexual relatives, they seem to be unsuccessful over the long term and to have short evolutionary lifespans [1,2]. Nevertheless, parthenogenetic species are distributed in many geographical areas where tend to occupy habitats characterized by unstable conditions [3]. One possible interpretation for this is that disturbed areas provide refuges where the contact with bisexual species is prevented, and this favours the settlement and establishment of parthenogenetic species. Alternatively, the preferential occupancy of disturbed areas might be because the parthenogens benefit from recurrent environmental stress. Their abundance in catastrophic or disturbed habitats can be easily attributed to their ability of colonization, but, under the continuous struggle between competitors, predators and parasites, parthenogens are expected to be doomed.

Bdelloid rotifers constitute the largest, oldest, most diverse animal taxon for which there is morphological, cytological, and molecular evidence for long-term parthenogenesis [4-9]. The group has likely evolved after having acquired the ameiotic reproduction as supported by recent results on the evolution of bdelloid genomes [e.g. [5,6]]. In spite of its conservative reproductive modality, taxon Bdelloidea has been able to evolve and differentiate into a few hundreds of distinguishable morphologies, traditionally considered species [10], which occupy a variety of freshwater habitats in all continents [11].

The sediments of lotic and lentic waters, as well as the thin water film around soil particles, mosses and lichens are bdelloids' common habitats, where temperature, food availability, chemical conditions and water content change quickly and unpredictably. The instability and uncertainty seem to favour bdelloid presence, as about 90% of the known species (about 400) occur in 'terrestrial' habitats [12]. In response to environmental stress, like desiccation or starvation, bdelloids enter dormancy and at recovery do not show either decreased fecundity or early death [13,14]. Recent work indicates that, for some species, mothers that have been through desiccation produce daughters of increased fitness and longevity, suggesting the existence of some repair processes associated with recovery from desiccation which may have a beneficial effect beyond surviving desiccation [15]. Some indirect experimental evidence seem to point to the same direction; a part of a clonal culture of a bdelloid species, Philodina roseola, was maintained under constantly hydrated conditions, and another part was desiccated. After recovery, both lines were checked and those recovered were found to have higher fertility [11].

It has been suggested that the unusual ecology of bdelloids, that through dormancy can cause frequent DNA damage and repair, may have facilitated adaptations that favoured their long term evolutionary survival in absence of sexual reproduction and of recombination [16]. If this is true, a bdelloid population should be predicted to have a higher fitness under severe stress than a parallel 'unstressed' line. We intend to test this hypothesis by comparing the life-history traits of two lines, one stressed repeatedly and another continuously unstressed, of two bdelloid species, Macrotrachela quadricornifera Milne, 1886, family Philodinidae, (called M.q.), and Adineta ricciae Segers & Shiel, 2005, family Adinetidae, (called A.r.). Both species live in habitats where desiccation occurs, are naturally capable of anhydrobiosis, a form of dormancy induced by water loss, and at re-hydration appear to ignore the time spent dry [15]. A.r. was originally collected from the dry sediments of an Australian billabong, at re-hydration recovers in high percentages and seems to increase its fecundity when compared to a parallel hydrated control [15,17,18]. M.q. was isolated from a moss around a spring-fed pond in Northern Italy, is cultivated in the lab since several years and after recovery has same fecundity as its hydrated control [13,19].

From a laboratory clonal culture of either species two subpopulations were isolated; one was maintained under continuous hydration for 15 months ("hydrated line" H), and the other one was desiccated for 7 days at monthly intervals ("desiccated line" D). For the D line of both species recovery percentages were assessed at each re-hydration. The 15 month experiment was repeated in two different years. The effect of desiccation on population fitness was assessed by running life-table experiments on cohorts established from the ancestor population (M0, used for reference) and from the H and D lines after four (M4), eight (M8), and twelve (M12) subsequent desiccations, that correspond to 4, 8, and 12 months respectively.

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