Skip to main content
Log in

Rapid adaptation of Brachionus angularis (Rotifera) to invasion by Brachionus calyciflorus

  • ROTIFERA XV
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

To test the hypothesis that Brachionus angularis can rapidly develop local adaptation to invasion by other monogonont rotifers, replicate populations of B. angularis were exposed to two environments invaded by B. calyciflorus at different inoculation densities and an environment free from invaders. During the selection experiment, the density of each population was reduced to starting conditions every 3 days, and the changes in population growth rate and mictic ratio of B. angularis were continuously tracked. During the 81-day (69 asexual generations) period of selection, the B. angularis populations in the environments with invaders showed a significant increase in growth rate but a non-significant change in mictic ratio over time when compared with those in the environment without invaders. A common garden experiment revealed that when exposed to the environments with invaders, the B. angularis populations evolved in the environments with invaders had higher growth rates than those evolved in the environment without invaders, and the opposite was also true, indicating that local adaptation was rapidly formed. Info-chemicals released by invaders to the environment might increase the heritability of higher growth rates, and thus facilitate the local adaptation of B. angularis populations to invasion by B. calyciflorus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alcantara-Rodriguez, J., J. Ciros-Pérez, E. Ortega-Mayagoitia, C. R. Serrania-Soto & E. Piedra-Ibarra, 2012. Local adaptation in populations of a Brachionus group plicatilis cryptic species inhabiting three deep crater lakes in Central Mexico. Freshwater Biology 57: 728–740.

    Google Scholar 

  • Aránguiz-Acuña, A. & R. Ramos-Jiliberto, 2014. Diapause may promote coexistence of zooplankton competitors. Journal of Plankton Research 36: 978–988.

    Google Scholar 

  • Becks, L. & A. F. Agrawal, 2010. Higher rates of sex evolve in spatially heterogeneous environments. Nature 468: 89–92.

    CAS  PubMed  Google Scholar 

  • Becks, L. & A. F. Agrawal, 2011. The effect of sex on the mean and variance of fitness in facultatively sexual rotifers. Journal of Evolutionary Biology 24: 656–664.

    CAS  PubMed  Google Scholar 

  • Becks, L. & A. F. Agrawal, 2012. The evolution of sex is favored during adaptation to new environments. PLoS Biology 10: e1001317.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Becks, L. & A. F. Agrawal, 2013. Higher rates of sex evolve under K-selection. Journal of Evolutionary Biology 26: 900–905.

    CAS  PubMed  Google Scholar 

  • Bennett, W. N. & M. E. Boraas, 1989. A demographic profile of the fastest growing metazoan: a strain of Brachionus calyciflorus (Rotifera). Oikos 55: 365–369.

    Google Scholar 

  • Bonsall, M. B. & M. P. Hassell, 1997. Apparent competition structures ecological assemblages. Nature 388: 371–373.

    CAS  Google Scholar 

  • Campillo, S., E. M. Garcia-Roger, M. J. Carmona, A. Gómez & M. Serra, 2009. Selection on life-history traits and genetic population divergence in rotifers. Journal of Evolutionary Biology 22: 2542–2553.

    CAS  PubMed  Google Scholar 

  • Campillo, S., E. M. Garcia-Roger, M. J. Carmona & M. Serra, 2011. Local adaptation in rotifer populations. Evolutionary Ecology 25: 933–947.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Carmona, M. J., N. Dimas-Flores, E. M. Garcia-Roger & M. Serra, 2009. Selection of low investment in sex in a cyclically parthenogenetic rotifer. Journal of Evolutionary Biology 22: 1975–1983.

    CAS  PubMed  Google Scholar 

  • Chase, J. M., P. A. Abrams & J. P. Grover, 2002. The interaction between predation and competition: a review and synthesis. Ecology Letters 5: 302–315.

    Google Scholar 

  • Ciros-Pérez, J., M. J. Carmona & M. Serra, 2002. Resource competition and patterns of sexual reproduction in sympatric sibling rotifer species. Oecologia 131: 35–42.

    PubMed  Google Scholar 

  • Cody, M. L. & J. M. Diamond, 1975. Ecology and Evolution of Communities. Harvard University Press, Cambridge.

    Google Scholar 

  • Conn, D. B., 2014. Aquatic invasive species and emerging infectious disease threats: a one health perspective. Aquatic Invasions 9: 383–390.

    Google Scholar 

  • Declerck, A. J. S. & S. Papakostas, 2017. Monogonont rotifers as model systems for the study of micro-evolutionary adaptation and its eco-evolutionary implications. Hydrobiologia 796: 131–144.

    Google Scholar 

  • Declerck, S. A. J., A. R. Malo, S. Diehl, D. Waasdorp, K. D. Lemmen, K. Proios & S. Papakostas, 2015. Rapid adaptation of herbivore consumers to nutrient limitation: eco-evolutionary feedbacks to population demography and resource control. Ecology Letters 18: 553–562.

    PubMed  Google Scholar 

  • Diamond, J. M. & T. J. Case, 1986. Community Ecology. Harper & Row, New York.

    Google Scholar 

  • Dumont, H. J., 1994. Ancient lakes have simplified pelagic food webs. Archiv für Hydrobiologie Beih 44: 223–234.

    Google Scholar 

  • Fussmann, G. F., 2011. Rotifers: excellent subjects for the study of macro- and micro-evolutionary change. Hydrobiologia 662: 11–18.

    Google Scholar 

  • Fussmann, G. F., S. P. Ellner & N. G. Hairston, 2003. Evolution as a critical component of plankton dynamics. Proceedings of the Royal Society B – Biological Sciences of United States of America 270: 1015–1022.

    Google Scholar 

  • Garcia-Roger, E. M., M. J. Carmona & M. Serra, 2005. Deterioration patterns in diapausing egg banks of Brachionus (Muller, 1786) rotifer species. Journal of Experimental Marine Biology and Ecology 314: 149–161.

    Google Scholar 

  • Gilbert, J. J., 1963. Mictic female production in the rotifer Brachionus calyciflorus. Journal of Experimental Zoology 153: 113–124.

    Google Scholar 

  • Gilbert, J. J., 1974. Dormancy in rotifers. Transactions of the American Microscopical Society 93: 490–513.

    Google Scholar 

  • Gilbert, J. J., 1980. Further observations on developmental polymorphism and its evolution in the rotifer Brachionus calyciflorus. Freshwater Biology 10: 281–294.

    Google Scholar 

  • Gilbert, J. J., 1988. Suppression of rotifer populations by Daphnia: a review of the evidence, the mechanisms, and the effects on zooplankton community structure. Limnology and Oceanography 33: 1286–1303.

    Google Scholar 

  • Gilbert, J. J., 2003. Specificity of crowding response that induces sexuality in the rotifer Brachionus. Limnology and Oceanography 48: 1297–1303.

    Google Scholar 

  • Guo, R., T. W. Snell & J. Yang, 2011. Ecological strategy of rotifer (Brachionus calyciflorus) exposed to predator- and competitor-conditioned media. Hydrobiologia 658: 163–171.

    Google Scholar 

  • Hagiwara, A., M.-M. Jung, T. Sato & K. Hirayama, 1995. Interspecific relations between marine rotifer Brachionus rotundiformis and zooplankton species contaminating in the rotifer mass culture tank. Fisheries Science 61: 623–627.

    CAS  Google Scholar 

  • Havel, J. E., K. E. Kovalenko, S. M. Thomaz, S. Amalfitano & L. B. Kats, 2015. Aquatic invasive species: challenges for the future. Hydrobiologia 750: 147–170.

    Google Scholar 

  • Hereford, J., 2009. A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist 173: 579–588.

    PubMed  Google Scholar 

  • Hu, H.-Y. & Y.-L. Xi, 2008. Demographic parameters and mixis of three Brachionus angularis Gosse (Rotatoria) strains fed on different algae. Limnologica 38: 56–62.

    Google Scholar 

  • Jung, M.-M., A. Hagiwara & K. Hirayama, 1997. Interspecific interactions in the marine rotifer microcosm. Hydrobiologia 358: 121–126.

    Google Scholar 

  • Kawecki, T. J. & D. Ebert, 2004. Conceptual issues in local adaptation. Ecology Letters 7: 1225–1241.

    Google Scholar 

  • Kirk, K. L., 1998. Enrichment can stabilize population dynamics: autotoxins and density dependence. Ecology 79: 2456–2462.

    Google Scholar 

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

    Google Scholar 

  • Li, S. H., H. Zhu, Y. Z. Xia, M. J. Yu, K. S. Liu, Z. Y. Ye & Y. X. Chen, 1959. The mass culture of unicellular green algae. Acta Hydrobiologica Sinica 4: 462–472.

    Google Scholar 

  • Lucía-Pavón, E., S. S. S. Sarma & S. Nandini, 2001. Effect of different densities of live and dead Chlorella vulgaris on the population growth of rotifers Brachionus calyciflorus and Brachionus patulus (Rotifera). Revista de Biología Tropical 49: 895–902.

    PubMed  Google Scholar 

  • Maeda, M. & A. Hino, 1991. Environmental management for mass culture of rotifer, Brachionus plicatilis. In Fulks, W. & K. L. Main (eds), Rotifer and Microalgae Culture Systems. Proceedings of a U.S.–Asia Workshop. The Oceanic Institute, Honolulu: 125–133.

    Google Scholar 

  • Marcus, N. H., R. Lutz, W. Burnett & P. Cable, 1994. Age, viability and vertical distribution of zooplankton resting eggs from an anoxic basin: evidence of an egg bank. Limnology and Oceanography 39: 154–158.

    Google Scholar 

  • Martínez-Ruiz, C. & E. M. García-Roger, 2015. Being first increases the probability of long diapause in rotifer resting eggs. Hydrobiologia 745: 111–121.

    Google Scholar 

  • Michaloudi, E., S. Papakostas, G. Stamou, V. Neděla, E. Tihlařiková, W. Zhang & S. A. J. Declerck, 2018. Reverse taxonomy applied to the Brachionus calyciflorus cryptic species complex: morphometric analysis confirms species delimitations revealed by molecular phylogenetic analysis and allows the (re)description of four species. PLoS ONE. https://doi.org/10.1371/journal.pone.0203168.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitchell, S. E. & G. R. Carvalho, 2002. Comparative demographic impacts of ‘info-chemicals’ and exploitative competition: an empirical test using Daphnia magna. Freshwater Biology 47: 459–471.

    Google Scholar 

  • Moran, N. A. & D. B. Sloan, 2015. The hologenome concept: helpful and hollow? PLoS Biology 13: e1002311.

    PubMed  PubMed Central  Google Scholar 

  • Morin, P. J., 2011. Community Ecology, 2nd ed. Wiley-Blackwell, Oxford.

    Google Scholar 

  • Poole, R. W., 1974. An Introduction to Quantitative Ecology. McGraw-Hill, New York.

    Google Scholar 

  • Pourriot, R., 1963. Influence du rythme nycthéméral sur le cycle sexual de quelques Rotifères. Comptes Rendus de I’Académie des Sciences Paris 256: 5216–5219.

    Google Scholar 

  • Pourriot, R. & T. W. Snell, 1983. Resting eggs in rotifers. Hydrobiologia 104: 213–224.

    Google Scholar 

  • Rebolledo, U. A., S. Nandini, S. S. S. Sarma, J. C. R. Reyes & G. A. R. M. De` Oca, 2018. Demographic and competition studies on Brachionus ibericus and Proales similis in relation to salinity and algal (Nannochloropsis oculata) density. Aquaculture International 26: 629–644.

    Google Scholar 

  • Reguera, B., 1984. The effect of ciliate contamination in mass cultures of the rotifer, Brachionus plicatilis O. F. Müller. Aquaculture 40: 103–108.

    Google Scholar 

  • Sarma, S. S. S. & S. Nandini, 2002. Comparative life table demography and population growth of Brachionus macracanthus Daday, 1905 and Platyias quadricornis Ehrenberg, 1832 (Rotifera, Brachionidae) in relation to algal (Chlorella vulgaris) food density. Acta Hydrochim Hydrobiologie 30: 128–140.

    CAS  Google Scholar 

  • Sarma, S. S. S. & S. Nandini, 2018. Allelopathic interactions in freshwater ecosystems with special reference to zooplankton. In Kaul, B. L., P. L. Koul & A. K. Verma (eds), Advances in Fish and Wildlife Ecology and Biology, Vol. 7. Astral International Pvt. Ltd., New Delhi: 195–221.

    Google Scholar 

  • Sarma, S. S. S., N. Iyer & H. J. Dumont, 1996. Competitive interactions between herbivorous rotifers: importance of food concentration and initial population density. Hydrobiologia 331: 1–7.

    Google Scholar 

  • Sarma, S. S. S., M. A. Fernández & S. Nandini, 1999. Competition between Brachionus calyciflorus Pallas and Brachionus patulus (Müller) (Rotifera) in relation to algal food concentration and initial population density. Aquatic Ecology 33: 339–345.

    Google Scholar 

  • Sarma, S. S. S., S. A. Rivera & F. E. Hinojosa, 2007. Combined influence of food level and inoculation density on competition between Anuraeopsis fissa and Brachionus patulus or Brachionus macracanthus (Rotifera: Brachionidae). Russian Journal of Ecology 38: 353–362.

    Google Scholar 

  • Sarma, S. S. S., J. A. Guevara-Franco, B. Almaraz-Ornelas & S. Nandini, 2018. Interspecific effects of allelochemicals of 4-species of Brachionidae (Rotifera: Monogononta) on the population growth. Allelopathy Journal 45: 277–290.

    Google Scholar 

  • Scheuerl, T. & C.-P. Stelzer, 2013. Patterns and dynamics of rapid local adaptation and sex in varying habitat types in rotifers. Ecology and Evolution 3: 4253–4264.

    PubMed  PubMed Central  Google Scholar 

  • Schoener, W. T., 2011. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331: 426–429.

    CAS  PubMed  Google Scholar 

  • Schröder, A., A. van Leeuwen & T. C. Cameron, 2014. When less is more: positive population-level effects of mortality. Trends in Ecology and Evolution 29: 614–624.

    PubMed  Google Scholar 

  • Simões, P., M. R. Rose, A. Duarte, R. Goncalves & M. Matos, 2007. Evolutionary domestication in Drosophila subobscura. Journal of Evolutionary Biology 20: 758–766.

    PubMed  Google Scholar 

  • Smith, H. A. & T. W. Snell, 2012. Rapid evolution of sex frequency and dormancy as hydroperiod adaptations. Journal of Evolutionary Biology 25: 2501–2510.

    CAS  PubMed  Google Scholar 

  • Smith, H. A. & T. W. Snell, 2014. Differential evolution of lifespan and fecundity between asexual and sexual females in a benign environment. International Review of Hydrobiology 99: 117–124.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Starkweather, P. L., J. J. Gilbert & T. M. Frost, 1980. Bacterial feeding by the rotifer Brachionus calyciflorus: clearance and ingestion rates, behavior and population dynamics. Oecologia 44: 26–30.

    Google Scholar 

  • Stelzer, C., 2005. Evolution of rotifer life histories. Hydrobiologia 546: 335–346.

    Google Scholar 

  • Stelzer, C.-P., 2011. The cost of sex and competition between cyclical and obligate parthenogenetic rotifers. The American Naturalist 177: E43–E53.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Stelzer, C. P. & T. W. Snell, 2006. Specificity of the crowding response in the Brachionus plicatilis species complex. Limnology and Oceanography 51: 125–130.

    Google Scholar 

  • Verschoor, A. M., Y. S. Zadereev & W. M. Mooij, 2007. Infochemical-mediated trophic interactions between the rotifer Brachionus calyciflorus and its food algae. Limnology and Oceanography 52: 2109–2119.

    CAS  Google Scholar 

  • Walczyńska, A., L. Franch-Gras & M. Serra, 2017. Empirical evidence for fast temperature-dependent body size evolution in rotifers. Hydrobiologia 796: 191–200.

    Google Scholar 

  • Walz, N., 1993. Plankton Regulation Dynamics. Springer, Berlin.

    Google Scholar 

  • Wang, M., Y.-L. Xi, B. Zhou & Y. Zhang, 2014. Adaptation of Brachionus calyciflorus (Rotifera) from Lake Jinghu in summer to water temperature: population growth experiment study. Acta Hydrobiologica Sinica 38: 1017–1023.

    Google Scholar 

  • Wen, X.-L., Y.-L. Xi, F.-P. Qian, G. Zhang & X.-L. Xiang, 2011. Comparative analysis of rotifer community structure in five subtropical shallow lakes in east China: role of physical and chemical conditions. Hydrobiologia 661: 303–316.

    CAS  Google Scholar 

  • Wen, X.-L., Y.-L. Xi, G. Zhang, Y.-H. Xue & X.-L. Xiang, 2016. Coexistence of cryptic Brachionus calyciflorus (Rotifera) species: roles of environmental variables. Journal of Plankton Research 38: 478–489.

    Google Scholar 

  • Yang, H. Q. & X. Y. Yang, 1996. Experimental studies on the culture of Brachionus angularis. Journal of Fisheries of China 20: 85–87.

    Google Scholar 

  • Zhang, Z. S. & X. F. Huang, 1991. Methods for Study on Freshwater Plankton. Science Press, Beijing.

    Google Scholar 

  • Zhang, Y., A. Zhou, Y.-L. Xi, Q. Sun, L.-F. Ning, P. Xie, X.-L. Wen & X.-L. Xiang, 2018. Temporal patterns and processes of genetic differentiation of the Brachionus calyciflorus (Rotifera) complex in a subtropical shallow lake. Hydrobiologia 807: 313–331.

    CAS  Google Scholar 

  • Zhu, G. L. & Z. M. Zhao, 2013. The preliminary study on artificial propagation and fry rearing of Misgurnus anguillicaudatus. Agricultural Science and Technology 8: 13–18.

    Google Scholar 

Download references

Acknowledgements

This work was funded by the Natural Science Foundation of China (31470015) and the Foundation of Provincial Key Laboratory of Biotic Environment and Ecological Safety in Anhui Province. We are grateful to the anonymous referees for their valuable comments and constructive suggestions, which have greatly improved the manuscript. We thank Catherine Dandie from Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), and Gen Zhang from Shenzhen Nobel Science and Technology Service Co., Ltd. for language editing service.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yi-Long Xi.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Guest editors: Steven A. J. Declerck, Diego Fontaneto, Rick Hochberg & Terry W. Snell / Crossing Disciplinary Borders in Rotifer Research

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 41 kb)

Supplementary material 2 (DOC 146 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xi, YL., Huang, KQ., Pan, L. et al. Rapid adaptation of Brachionus angularis (Rotifera) to invasion by Brachionus calyciflorus. Hydrobiologia 844, 31–42 (2019). https://doi.org/10.1007/s10750-019-3959-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-3959-y

Keywords

Navigation