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A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera)

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Abstract

The defining feature of the life cycle in monogonont rotifers such as Brachionus plicatilis (Muller) is alternation of asexual and sexual reproduction (mixis). Why sex is maintained in such life cycles is an important unsolved evolutionary question and one especially amenable to experimental analysis. Mixis is induced by a chemical signal produced by the rotifers which accumulates to threshold levels at high population densities. The chemical features of this signal were characterized using size exclusion, enzymatic degradation, protease protection assays, selective binding to anion ion exchange and C3 reversed phase HPLC columns, and the sequence of 17 N-terminal amino acids. These studies were carried out over two years beginning in 2003 using B. plicatilis Russian strain. When rotifer-conditioned medium was treated with proteinase K, its mixis-inducing ability was reduced by 70%. Proteinase K was added to medium auto-conditioned by 1 female ml−1 where typically 17% of daughters became mictic and mixis was reduced to 1%. A cocktail of protease inhibitors added to conditioned medium significantly reduced degradation of the mixis signal by natural proteases. Conditioned medium subjected to ultrafiltration retained mixis-inducing activity in the >10 kDa fraction, but the <10 kDa fraction had no significant activity. The putative mixis signal bound to an anion exchange column, eluting off at 0.72 M NaCl. These fractions were further separated on a C3 reversed phase HPLC column and mixis-inducing activity was associated with a 39 kDa protein. Seventeen amino acids from the N-terminus have strong similarity to a steroidogenesis-inducing protein isolated from human ovarian follicular fluid. The 39 kDa protein is an excellent candidate for the rotifer mixis induction signal.

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References

  • Boraas ME (1983) Population dynamics of food limited rotifers in two-stage chemostat culture. Limnol Oceanogr 28:546–563

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Buchner H (1941) Entwicklungsphyiologische Untersuchungen uber den Generationswechsel der Radertiere. 1. Einleitende Studien uber den Determinationspunkt. Wilhelm Roux Arch Entwicklung Organ 141:154–158

    Article  Google Scholar 

  • Carmona MJ, Serra M, Miracle MR (1993) Relationships between mixis in Brachionus plicatilis and preconditioning of culture medium by crowding. Hydrobiologia 255/256:145–152

    Article  Google Scholar 

  • Carmona MJ, Gomez A, Serra M (1995) Mictic patterns of Brachionus plicatilis in small ponds. Hydrobiologia 313/314:365–371

    Article  Google Scholar 

  • Derry AM, Hebert PDN, Prepas EE (2003) Evolution of rotifers in saline and subsaline lakes: A molecular phylogenetic approach. Limnol Oceanogr 48:675–685

    Article  CAS  Google Scholar 

  • Fussmann GF, Ellner SP, Hairston NG Jr. (2003) Evolution as a critical component of plankton dynamics. Proc R Soc Lond B 270:1015–1022

    Article  Google Scholar 

  • Garcia-Roger EM, Carmona MJ, Serra M (2005) Deterioration patterns in diapausing egg banks of Brachionus (Muller, 1786) rotifer species. J Exp Mar Biol Ecol 314:149–161

    Article  Google Scholar 

  • Gilbert JJ (1963) Mictic female production in the rotifer Brachionus calyciflorus. J Exp Zool 153:113–124

    Article  Google Scholar 

  • Gilbert JJ (1974) Dormancy in rotifers. Trans Am Microsc Soc 93:490–513

    Article  Google Scholar 

  • Gilbert JJ (1977) Mictic-female production in monogonont rotifers. Archiv für Hydrobiologie Beihefte 8:142–155

    Google Scholar 

  • Gilbert JJ (1983) Rotifera. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol I. Oogenesis, oviposition, and oosorption. Wiley, New York, pp 181–209

    Google Scholar 

  • Gilbert JJ (1988) Rotifera. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol IV, part A. Fertilization, development, and parental care. Oxford and IBH Publishing Company, New Delhi, pp 179–199

    Google Scholar 

  • Gilbert JJ (1993) Rotifera. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol VI, part A. Asexual propagation and reproductive strategies. Oxford and IBH Publishing Company, New Delhi, pp 231–263

    Google Scholar 

  • Gilbert JJ (2002) Natural regulation of environmentally-induced sexuality in a rotifer: a multigenerational parental effect induced by fertilization. Freshw Biol 47:1633–1641

    Article  Google Scholar 

  • Gilbert JJ (2003a) Specificity of crowding response that induces sexuality in the rotifer Brachionus. Limnol Oceangr 48:1297–1303

    Article  Google Scholar 

  • Gilbert JJ (2003b) Environmental and natural control of sexuality in a rotifer life cycle: developmental and population biology. Evol Dev 5:19–24

    Article  Google Scholar 

  • Gilbert JJ (2004) Population density, sexual reproduction and diapause in monogonont rotifers: new data for Brachionus and a review. J Limnol 63(suppl):32–36

    Google Scholar 

  • Gilbert JJ, Schröder T (2004) Rotifers from diapausing, fertilized eggs: Unique features and emergence. Limnol Oceanogr 49:1341–1354

    Article  Google Scholar 

  • Gilbert JJ, Walsh EJ (2005) Brachionus calyciflorus is a species complex: Mating behavior and genetic differentiation among four geographically isolated strains. Hydrobiologia 546:257–265

    Article  CAS  Google Scholar 

  • Gómez A, Temprano M, Serra M (1995) Ecological genetics of a cyclical parthenogen in temporary habitats. J Evol Biol 8:601–622

    Article  Google Scholar 

  • Gómez A, Carvalho GR, Lunt DH (2000) Phylogeography and regional endemism of a passively dispersing zooplankter: mtDNA variation of rotifer resting egg banks. Proc R Soc Lond B 267:2189–2197

    Article  Google Scholar 

  • Gómez A, Serra M, Carvalho GR, Lunt DH (2002) Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56:1431–1444

    PubMed  Google Scholar 

  • Gómez A, Adcock GA, Lunt DH, Carvalho GR (2002b) The interplay between colonization history and gene flow in passively dispersing zooplankton: microsatellite analysis of rotifer resting egg banks. J Evol Biol 15:158–171

    Article  Google Scholar 

  • Guillard RRL (1983) Culture of phytoplankton for feeding marine invertebrates. In: Berg CJ Jr (ed) Culture of marine invertebrates. Hutchinson Ross, Stroudsburg

    Google Scholar 

  • Hino A, Hirano R (1976) Ecological studies on the mechanism of bisexual reproduction in the rotifer Brachionus plicatilis—I. General aspects of bisexual reproduction inducing factors. Bull Jpn Soc Sci Fish 42:1093–1099

    Google Scholar 

  • Hino A, Hirano R (1977) Ecological studies on the mechanism of bisexual reproduction in the rotifer Brachionus plicatilis—II. Effects of cumulative parthenogenetic generation on the frequency of bisexual reproduction. Bull Jpn Soc Sci Fish 43:1147–1155

    Google Scholar 

  • Hobæk A, Larsson P (1990) Sex determination in Daphnia magna. Ecology 71:2255–2268

    Article  Google Scholar 

  • Kahn S, May P, Matisiak E, Reddy J, Konu O, Cheng Z, Millena A (2005) Isolation of human steroidogenesis-inducing protein from human ovarian follicular fluid (submitted)

  • Kleiven OT, Larsson P, Hobæk A (1992) Sexual reproduction in Daphnia magna requires three stimuli. Oikos 65:197–206

    Google Scholar 

  • Kotani T, Ozaki M, Matsuoka K, Snell TW, Hagiwara A (2001) Reproductive isolation among geographically and temporally isolated marine Brachionus populations. Hydrobiologia 446/447:283–290

    Article  Google Scholar 

  • Krieger J, Breer H (1999) Olfactory reception in invertebrates. Science 286:720–723

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ortells R, Snell TW, Gómez A, Serra M (2000) Patterns of genetic differentiation in resting egg banks of a rotifer species complex in Spain. Arch Hydrobiol 149:529–551

    Google Scholar 

  • Ortells R, Gómez A, Serra M (2003) Coexistence of cryptic rotifer species: ecological and genetic characterization of Brachionus plicatilis. Freshw Biol 48: 2194–2202

    Article  Google Scholar 

  • Pourriot R, Snell TW (1983) Resting eggs in rotifers. Hydrobiologia 104:213–224

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Ruttner-Kolisko A (1964) Uber der labile Periode im Fortpflanzungszyklus der Radertiere. Int Gesam Hydrobiol 49:473–482

    Google Scholar 

  • Schröder T, Gilbert JJ (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. Funct Ecol 18:458–466

    Article  Google Scholar 

  • Segers H (1998) An analysis of taxonomic studies on Rotifera: a case study. Hydrobiologia 387/388:9–14

    Article  Google Scholar 

  • Segers H (2002) The nomenclature of the Rotifera: annotated checklist of valid family-and genus-group names. J Nat Hist 36:631–640

    Article  Google Scholar 

  • Serra M, King CE (1999) Optimal rates of bisexual reproduction in cyclical parthenogens with density-dependent growth. J Evol Biol 12:263–271

    Article  Google Scholar 

  • Serra M, Galiana A, Gómez A (1997) Speciation in monogonont rotifers. Hydrobiologia 358:63–70

    Article  Google Scholar 

  • Serra M, Gómez A, Carmona MJ (1998) Ecological genetics of Brachionus sibling species. Hydrobiologia 387/388:373–384

    Article  Google Scholar 

  • Serra M, Snell TW, King CE (2004) 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

    Google Scholar 

  • Serra M, Snell TW, Gilbert JJ (2005) Delayed mixis in rotifers: an adaptive response to the effects of density-dependent sex on population growth. J Plankton Res 27:37–45

    Article  Google Scholar 

  • Shull AF (1912) Studies in the life cycle of Hydatina senta. III. Internal factors influencing the proportion of male-producers. J Exp Zool 12:283–317

    Article  Google Scholar 

  • Snell TW (1987) Sex, population dynamics and resting egg production in rotifers. Hydrobiologia 144:105–111

    Google Scholar 

  • Snell TW (1989) Systematics, reproductive isolation and species boundaries in monogonont rotifers. Hydrobiologia 186/187:299–310

    Article  Google Scholar 

  • Snell TW (1998) Chemical ecology of rotifers. Hydrobiologia 387/388:267–276

    Article  Google Scholar 

  • Snell TW, Hoff FH (1987) Fertilization and male fertility in the rotifer Brachionus plicatilis. Hydrobiologia 147:329–334

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. W.H. Freeman, New York

    Google Scholar 

  • Stelzer CP, Snell TW (2003) Induction of sexual reproduction in Brachionus plicatilis (Monogononta, Rotifera) by a density-dependent chemical cue. Limnol Oceanogr 48:939–943

    Article  Google Scholar 

  • Stelzer CP, Snell TW (2005) Sexual communication in an ancient species complex: Evolution of the mixis inducing signal in Brachionus plicatilis (Rotifer) (in press)

  • Stross RG, Hill JC (1965) Diapause induction in Daphnia requires two stimuli. Science 150:1463–1464

    Google Scholar 

  • Suatoni E, Vicario S, Rice S, Snell TW, Caccone A (2005) Phylogenetic and biogeographic patterns in the salt water rotifer, Brachionus plicatilis (submitted)

  • Taga ME, Bassler BL (2003) Chemical communication among bacteria. PNAS 100:14549–14554

    Article  PubMed  CAS  Google Scholar 

  • Wallace RL, Snell TW (2001) Rotifera. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates, 2nd edn. Academic, New York

    Google Scholar 

  • Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424:303–306

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank John Gilbert, Manuel Serra, and David Mark Welch for valuable comments that improved this paper. This work was supported by the National Science Foundation grants BE/GenEn MCB-0412674 to TWS and OCE-0134843 to JK. The Deutsche Forschungsgemeinschaft (STE 1021/1) supported CPS with a post-doctoral fellowship.

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Correspondence to Terry W. Snell.

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Communicated by J.P. Grassle, New Brunswick

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Snell, T.W., Kubanek, J., Carter, W. et al. A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Mar Biol 149, 763–773 (2006). https://doi.org/10.1007/s00227-006-0251-2

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  • DOI: https://doi.org/10.1007/s00227-006-0251-2

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