Immediate and heritable costs of desiccation on the life history of the bdelloid rotifer Philodina roseola
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The long-term persistence of the ‘ancient asexual’ bdelloid rotifers, a clade of small aquatic invertebrates, is often tied to their ability to enter anhydrobiosis. This ability has both clear benefits (e.g. survival of desiccating conditions), but offers considerable costs (e.g. subsequent repair of the genome as well as physiological and metabolic costs to re-establish the phenotype). Despite these costs, several studies show that the time spent dry is effectively ignored with respect to life expectancy (the Sleeping Beauty hypothesis) and that reconstruction of the genome after a desiccation event might even be necessary to repair mistakes accumulated in it from obligate parthenogenesis while the animals were active. We propose that this genomic repair might not derive exclusively because desiccation per se, but could also result from genetic exchange that appears to occur between individuals during this time. By comparing individuals of Philodina roseola Ehrenberg, 1832 desiccated in groups versus individually, we document costs to desiccation in the isolated treatment group that impact negatively on lifespan and reproduction. In addition, comparing both groups with continuously active individuals reveals no strong evidence for the Sleeping Beauty hypothesis in this species nor any decline in fitness over a six-month period for the latter group. Finally, many treatment effects are at least partly heritable and were found in the untreated F1 generations. In particular, individuals desiccated in groups and their offspring could both reproduce faster than the offspring of continuously active individuals. Thus, our results offer additional support for the hypothesis of genetic exchange occurring during desiccation events in P. roseola and highlight the importance of considering this factor, and desiccation in general, in explaining bdelloid fitness. Moreover, our results provide additional context for understanding how the genetic information of bdelloids is ultimately shaped.
KeywordsAnhydrobiosis Fitness Genetic exchange Genomic repair Reproductive output Sleeping beauty hypothesis
The authors thank David B. Mark Welch for providing the P. roseola culture, Claus-Peter Stelzer for the algae as well as assistance and material for maintaining rotifers in the lab, Gerhard Zotz for the use of his Snijders scientific B.V. ECP01E, the electronic workshop of the University of Oldenburg for building the humido-thermostatic chambers, and Kornelius Rohmeyer for statistical advice. R.L. Wallace also provided numerous comments to help improve the manuscript.
This work was supported by the German Science Foundation (DFG) grant BI 825/6–1.
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Conflict of interest
The authors declare that they have no competing interests.
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