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.
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References
Aparici E, Carmona MJ, Serra M (1998) Sex allocation in haplodiploid cyclical parthenogens with density-dependent proportion of males. Am Nat 152: 652–657
Aparici E, Carmona MJ, Serra M (2002) Evidence for an even sex allocation in haplodiploid cyclical parthenogens. J Evol Biol 15:65–73
Armengol X, Boronat L, Camacho A, Wurtsbaugh W (2001) Grazing by a dominant rotifer Conochilus unicornis Rousselet in a mountain lake: In situ measurements with synthetic microspheres. Hydrobiologia 446/447: 107–114
Bennet WN, Boraas ME (1989) A demographic profile of the fastest growing metazoan – a strain of Brachionus calyciflorus (Rotifera). Oikos 55: 365–369
Boraas ME (1983) Population dynamics of food-limited rotifers in two-stage chemostat culture. Limnol Oceanogr 28: 546–563
Bray S, Amrein H (2003) A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39: 1019–1029
Caprioli M, Ricci C (2001) Recipies for successful aanhydrobiosis in bdelloid rotifers. Hydrobiologia 446/447: 13–17
Colbourne JK, Hebert PDN (1996) The systematics of North American Daphnia (Crustacea: Anomopoda): a molecular phylogenetic approach. Philos Trans R Soc Lond 351: 349–360
Crease TJ, Stanton DJ, Hebert PDN (1989) Polyphyletic origins of asexuality in Daphnia pulex II. Mitochondrial-DNA variation. Evolution 43: 1016–1026
Fussmann GF, Ellner SP, Hairston NG Jr (2003) Evolution as a critical component of plankton dynamics. Proc R Soc Lond B 270: 1015–1022
Garcia-Roger EM, Carmona MJ, Serra M (2006) Patterns in rotifer diapausing egg banks: density and viability. J Exp Mar Biol Ecol 336: 198–210
Gilbert JJ (1963) Mictic female production in the rotifer Brachionus calyciflorus. J Exp Zool 153: 113–124
Gilbert JJ (1995) Structure, development and induction of a new diapause stage in rotifers. Freshw Biol 34: 263–270
Gilbert JJ (2002) Endogenous regulation of environmentally induced sexuality in a rotifer: a multigenerational parental effect induced by fertilisation. Freshw Biol 47: 1633–1641
Gilbert JJ (2003) Specificity of crowding response that induces sexuality in the rotifer Brachionus. Limnol Oceanogr 48: 1297–1303
Gómez A, Carvalho GR (2000) Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank populations. Mol Ecol 9: 203–214
Gómez A, Serra M, Carvalho GR, Lundt DH (2002) Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56: 1431–1445
Hebert PDN (1987) Genotypic characteristics of cyclic parthenogens and their obligately asexual derivatives. In: Stearns SC (ed) The evolution of sex and its consequences. Birkhauser Verlag, Basel and Boston, pp. 175–195
Innes DJ, Hebert PDN (1988) The origin and genetic basis of obligate parthenogenesis in Daphnia pulex. Evolution 42: 1024–1035
King CE (1980) The genetic structure of zooplankton populations. In: Kerfoot WC (ed). Evolution and ecology of zooplankton communities. University Press of New England, Hanover, pp. 315–329
King CE, Snell TW (1977) Genetic basis of amphoteric reproduction in rotifers. Heredity 39: 361–364
Kotani T, Ozaki M, Matsuoka K, Snell TW, Hagiwara A (2001) Reproductive isolation among geographically and temporally isolated marine Brachionus strains. Hydrobiologia 446/447: 283–290
Kubanek J, Snell TW (2008) Quorum sensing in rotifers. In: Winans SC, Bassler BL (eds). Chemical communication among bacteria. ASM Press, Washington DC, pp. 453–461
Lynch M, Deng HW (1994) Genetic slippage in response to sex. Am Nat 144: 242–261
Marcus NH, Lutz R, Burnett W, Cable P (1994) Age, viability, and vertical distribution of zooplankton resting eggs from an anoxic basin: evidence of an egg bank. Limnol Oceanogr 39: 154–158
Mark Welch DB, Cummings MP, Hillis DM, Meselson M (2004a) When do gene copies in the asexual class Bdelloidea diverge? Proc Natl Acad Sci USA 101: 1622–1625
Mark Welch DB, Meselson M (2000) Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211–1215
Mark Welch DB, Meselson M (2001) Rates of nucleotide substitution in sexual and ancient asexual rotifers. Proc Natl Acad Sci USA 98: 6720–6724
Mark Welch, JL, Mark Welch DB, Meselson M (2004b) Cytogenetic evidence for asexual evolution of bdelloid rotifers. Proc Natl Acad Sci USA 101: 1618–1621
Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge, UK
Maynard Smith J (1986) Contemplating life without sex. Nature 324: 300–301
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165–199
Moran NA (1992) The evolution of aphid life cycles. Annu Rev Entomol 27: 321–348
Normark BB, Judson OP, Moran NA (2003) Genomic signatures of ancient asexual lineages. Biol J Linnean Soc 79: 69–84
Ortells R, Gomez A, Serra M (2006) Effects of duration of the planktonic phase on rotifer genetic diversity. Arch Hydrobiol 167: 203–216
Peck J, Waxman D (2000) What’s wrong with a little sex? J Evol Biol 13: 63–69
Pourriot R, Clément P (1981) Action de facteurs externes sur la reproduction et le cycle reproducteur des Rotifers. Acta Oecologica Generale 2: 135–151
Ricci C, Melone G (1998) Dwarf males in monogonont rotifers. Aquatic Ecol 32: 361–365
Schröder T, Howard S, Arroyo ML, Walsh EJ (2007) Sexual reproduction and diapause of Hexarthra sp (Rotifera) in short-lived ponds in the Chihuahuan Desert. Freshw Biol 52: 1033–1042
Serra M, Carmona MJ (1993) Mixis strategies and resting egg production of rotifers living in temporally-varying habitats. Hydrobiologia 255–256: 117–126
Serra M, King CE (1999) Optimal rates of bisexual reproduction in cyclical parthenogens with density-dependent growth. J Evol Biol 12: 263–271.
Serra M, Snell TW, King CE (2003) The timing of sex in cyclically parthenogenetic rotifers. In: Moya A, Font E (eds) Evolution: from molecules to ecosystems. Oxford University Press, New York, pp. 135–146.
Simon JC, Delmotte F, Rispe C, Crease T (2003) Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol J Linn Soc 79: 151–163
Simon JC, Rispe C, Sunnucks P (2002) Ecology and evolution of sex in aphids. Trends Ecol Evol 17: 34–39
Snell TW (1987) Sex, population dynamics and resting egg production in rotifers. Hydrobiologia 144: 105–111
Snell TW (1989) Systematics, reproductive isolation and species boundaries in monogonont rotifers. Hydrobiologia 186/187: 299–310
Snell TW, Boyer EM (1988) Thresholds for mictic female production in the rotifer Brachionus plicatilis (Muller). J Exp Mar Biol Ecol 124: 73–85
Snell TW, Kubanek J, Carter J, Payne AB, Kim J, Hicks MK, Stelzer CP (2006) A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Mar Biol 149: 763–773
Snell TW, Serra M, Carmona MJ (1998) Toxicity and sexual reproduction in rotifers: reduced resting egg production and heterozygosity loss. In: Forbes VE (ed) Genetics and Ecotoxicology. Taylor and Francis, London, pp. 169–185
Stelzer CP (2008) Obligate asexuality in a rotifer and the role of sexual signals. J Evol Biol 21: 287–293
Stelzer CP, Snell TW (2003) Induction of sexual reproduction in Brachionus plicatilis (Monogononta, Rotifera) by low density-dependent chemical cue. Limnol Oceanogr 48: 939–943
Stelzer CP, Snell TW (2006) Specificity of the crowding response in the Brachionus plicatilis species complex. Limnol Oceanogr 51: 125–130
Suatoni E, Vicario S, Rice S, Snell TW, Caccone A (2006) An analysis of species boundaries and biogeographic patterns in a cryptic species complex: the rotifer Brachionus plicatilis. Mol Phyl Evol 41: 86–98
Tagg N, Doncaster CP, Innes DJ (2005) Outcomes of reciprocal invasions between genetically diverse and genetically uniform populations of Daphnia obtusa (Kurz). Oecologia 143: 527–536
Wallace RL, Snell TW, Ricci C, Nogrady T (2006) Rotifera 1: Biology, Ecology and Systematics. Backhuys Publishers, Leiden
Williams GC (1975) Sex and Evolution. Princeton University Press, Princeton
Yoshida T, Jones LE, Ellner S, Fussmann GF, Hairston NG Jr (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424: 303–306
Acknowledgements
We thank Maria José Carmona for valuable comments that improved this paper. Two anonymous reviewers made useful comments that we incorporated into this chapter. This work was supported by the National Science Foundation grants BE/GenEn MCB-0412674 to TWS and by the Spanish Ministry of Education and Science grants CLG2006-27069-E/BOS and BOS2003-0075 to MS.
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Serra, M., Snell, T.W. (2009). Sex Loss in Monogonont Rotifers. In: Schön, I., Martens, K., Dijk, P. (eds) Lost Sex. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2770-2_14
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DOI: https://doi.org/10.1007/978-90-481-2770-2_14
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