Abstract
The effect of starvation on sexual reproduction in cyclic parthenogenetic rotifers has been studied using life history experiment. Short-time starvation of rotifers that experienced starvation immediately after hatching from resting eggs can cause high induction of sexual reproduction up to the 10th generation. However, it is not clear whether the induction of sexual reproduction can occur beyond the 10th generation. To investigate this phenomenon, we conducted a sex induction study using the monogonont rotifer Brachionus manjavacas. Newborn stem females were starved for 12 h, while controls were supplied with 7.0 × 106 cells ml−1 of Nannochloropsis oculata. In a life history experiment, the rotifers were individually cultured in 96-well microplates containing 0.2 ml of seawater (22 ppt) in each well at 25 °C with daily feeding thereafter. Mixis induction in offspring from starved stem females was significantly higher than in those from non-starved stem females up to the 40th generation. The effect of accumulative generations increased mixis induction up to the 20th generation. Effect on future generations of the rise in mixis ratio by the starvation to stem females may facilitate colonization by favoring population growth via female parthenogenesis and by decreasing food requirements for survival and reproduction.
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References
Bird, A., 2002. DNA methylation patterns and epigenetic memory. Genes & Development 16: 6–21.
Fussmann, G. F., G. Kramer & M. Labib, 2007. Incomplete induction of mixis in Brachionus calyciflorus: patterns of reproduction at the individual level. Hydrobiologia 593: 111–119.
Gilbert, J. J., 1963. Mictic female production in the rotifer Brachionus calyciflorus. Journal of Experimental Zoology 153: 113–124.
Gilbert, J. J., 2003. Specificity of crowding response that induces sexuality in the rotifer Brachionus. Limnology and Oceanography 48: 1297–1303.
Gilbert, J. J. & T. Schröder, 2004. Rotifers from diapausing, fertilized eggs: unique features and emergence. Limnology & Oceanography 49: 1341–1354.
Hagiwara, A. & A. Hino, 1989. Effects of incubation and preservation on resting egg hatching and mixis in the derived clones of the rotifer Brachionus plicatilis. Hydrobiologia 186(187): 412–415.
Hagiwara, A. & A. Hino, 1990. Feeding history and hatching of resting eggs in the marine rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 56: 1901–1907.
Hagiwara, A., A. Hino & R. Hirano, 1988. Effects of temperature and chlorinity on resting egg formation in the Rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 54: 569–575.
Hagiwara, A., K. Hamada, S. Hori & K. Hirayama, 1994. Increased sexual reproduction in Brachionus plicatilis (Rotifera) with the addition of bacterial and rotifer extracts. Journal of Experimental Marine Biology and Ecology 181: 1–8.
Hagiwara, A., W. G. Gallardo, M. Assavaaree, T. Kotani & A. B. de Araujo, 2001. Live food production in Japan: recent progress and future aspects. Aquaculture 200: 111–127.
Hagiwara, A., Y. Kadota & A. Hino, 2005. Maternal effect by stem females in Brachionus plicatilis: effect of starvation on mixis induction in offspring. Hydrobiologia 546: 275–279.
Hino, A. & R. Hirano, 1976. Ecological studies on the mechanism of bisexual reproduction in the rotifer Brachionus plicatilis – I. General aspects of bisexual reproduction inducing factors. Nippon Suisan Gakkaishi 42: 1093–1099.
Hino, A. & R. Hirano, 1977. Ecological studies of the mechanism of bisexual reproduction in the rotifer Brachionus plicatilis – II. Effects of cumulative parthenogenetic generation on the frequency of bisexual reproduction. Nippon Suisan Gakkaishi 43: 1147–1155.
Hino, A. & R. Hirano, 1984. Relation between water temperature and bisexual reproduction rate in the rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 50: 1481–1485.
Hino, A. & R. Hirano, 1985. Relationship between the temperature given at the time of fertilized egg formation and bisexual reproduction pattern in the deriving strain of the rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 51: 511–514.
Hino, A. & R. Hirano, 1988. Relationship between water chlorinity and bisexual reproduction rate in the rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 54: 1329–1332.
Hirayama, K., K. Takagi & H. Kimura, 1979. Nutritional effect of eight species of marine phytoplankton on population growth of the rotifer, Brachionus plicatilis. Nippon Suisan Gakkaishi 45: 11–16.
Kim, B.-M., L. Mirbahai, A. Mally, J. K. Chipman, J. S. Rhee & J. S. Lee, 2016. Correlation between the DNA methyltransferase (Dnmt) gene family and genome-wide 5-methylcytosine (5mC) in rotifer, copepod, and fish. Genes & Genomics 38: 13–23.
Korstad, J., Y. Olsen & O. Vadstein, 1989. Life history characteristics of Brachionus plicatilis (Rotifera) fed different algae. Hydrobiologia 186: 46–50.
Lubzens, E., R. Fishler & V. Berdugo-White, 1980. Induction of sexual reproduction and resting egg production in Brachionus plicatilis reared in sea water. Hydrobiologia 73: 55–58.
Lubzens, E., G. Minkoff & S. Marom, 1985. Salinity dependence of sexual and asexual reproduction in the rotifer Brachionus plicatilis. Marine Biology 85: 123–126.
Lubzens, E., A. Tandler & G. Minkoff, 1989. Rotifers as food in aquaculture. Hydrobiologia 186(187): 387–400.
Rothhaupt, O. K., 1995. Algal nutrient limitation affects rotifer growth rate but not ingestion rate. Limnology and Oceanography 40: 1201–1208.
Schröder, T. & J. J. Gilbert, 2004. Transgenerational plasticity for sexual reproduction and diapause in the life cycle of monogonont rotifers: Intraclonal, intraspecific and interspecific variation in the response to crowding. Functional Ecology 18: 458–466.
Schröder, T., S. Howard, L. Arroyo & E. J. Walsh, 2007. Sexual reproduction and diapause of Hexarthra sp. (Rotifera) in short-lived Chihuahuan Desert ponds. Freshwater Biology 52: 1033–1042.
Serra, M. & M. J. Carmona, 1993. Mixix strategies and resting egg production of rotifers living in temporary-varying habitats. Hydrobiologia 255(256): 117–126.
Snell, T. W., 1986. Effect of temperature, salinity and food level on sexual and asexual reproduction in Brachionus plicatilis (Rotifera). Marine Biology 92: 157–162.
Snell, T. W. & E. M. Boyer, 1988. Thresholds for mictic female production in the rotifer Brachionus plicatilis (Müller). Journal of Experimental Marine Biology and Ecology 124: 77–85.
Snell, T. W. & F. H. Hoff, 1985. The effect of environmental factors on resting egg production in the rotifer Brachionus plicatilis. Journal of World Mariculture Society 16: 484–497.
Snell, T. W., J. Kubanek, W. Carter, A. B. Payne, J. Kim, M. K. Hicks & C. P. Stelzer, 2006. A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Marine Biology 149: 763–773.
Stelzer, C. P. & T. W. Snell, 2003. Induction of sexual reproduction in Brachionus plicatilis (Monogononta, Rotifera) by a density-dependent chemical cue. Limnology and Oceanography 48: 939–943.
Wallace, R. L., T. Snell & H. A. Smith, 2015. Phylum Rotifera. In Thorp, J. H. & D. C. Rogers (eds), Thorp and Covich’s Freshwater Invertebrates. Elsevier, Waltham: 225–271.
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This study was supported by MEXT/JSPS KAKENHI Grant No. 24658174. The authors are extremely grateful to anonymous reviewers for taking their time to improve the quality of our manuscript.
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Guest editors: M. Devetter, D. Fontaneto, C. D. Jersabek, D. B. Mark Welch, L. May & E. J. Walsh / Evolving rotifers, evolving science
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Kamizono, S., Ogello, E.O., Sakakura, Y. et al. Effect of starvation and accumulation of generations on mixis induction in offspring of the monogonont rotifer Brachionus manjavacas hatched from resting eggs. Hydrobiologia 796, 93–97 (2017). https://doi.org/10.1007/s10750-016-3078-y
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DOI: https://doi.org/10.1007/s10750-016-3078-y