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Inter-genotype variation in reproductive response to crowding among Daphnia pulex

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Abstract

Crowding is known to have a major influence on reproduction in the freshwater microcrustacean Daphnia pulex. We analyzed reproductive output of six different D. pulex genotypes under two different density regimes in the laboratory. Four of these genotypes reproduce via obligate parthenogenesis, allowing thorough analysis of the life history strategies of some asexual lines. Among 30,109 neonate offspring and 1041 resting egg ephippia collected, several trends were evident. Crowding induced increased resting egg production and reduced neonate offspring production among all genotypes. Offspring sex ratios grew more male-biased with maternal age. The extent, but not direction, of each of these trends varied among genotypes. Offspring sex ratios, and the very direction in which they changed in response to crowding, differed significantly among genotypes with some genotypes producing more and others fewer males in response to crowding. Obligately parthenogenetic genotypes seemed to respond to the crowding stimulus in similar ways as the facultatively parthenogenetic genotypes, as expected from the sexual origins of their genomes. The inter-genotype variation in life-history traits observed in this and other investigations calls into question the common practice of extrapolating results from a single Daphnia genotype to an entire species. Our findings are considered in the context of other research in the field of environmental influences on Daphnia reproduction with a review of representative literature.

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References

  • Alekseev V. and Lampert W. (2001). Maternal control of resting-egg production in Daphnia. Nature 414: 899–901

    Article  PubMed  CAS  Google Scholar 

  • Antunes S. C., Castro B. B. and Gonçalves F. (2003). Chronic responses of different clones of Daphnia longispina (field and ephippia) to different food levels. Acta Oecologica 24: S325–S332

    Article  Google Scholar 

  • Baird D. J., Barber I., Bradley M., Soares A. M. V. M. and Calow P. (1991). A comparative study of genotype sensitivity to acute toxic stress using clones of Daphnia magna Straus. Ecotoxicology and Environmental Safety 21: 257–265

    Article  PubMed  CAS  Google Scholar 

  • Banta A. M. and Brown L. A. (1929). Control of sex in Cladocera. I. crowding the mothers as a means of controlling male production. Physiological Zoölogy 2: 80–92

    CAS  Google Scholar 

  • Barker D. M. and Hebert P. D. N. (1986). Secondary sex ratio of the cyclic parthenogen Daphnia magna (Crustacea: Cladocera) in the Canadian Arctic. Canadian Journal of Zoology 64: 1137–1143

    Google Scholar 

  • Bensch S., Westerdahl H., Hansson B. and Hasselquist D. (1999). Do females adjust the sex of their offspring in relation to the breeding sex ratio?. Journal of Evolutionary Biology 12: 1104–1109

    Article  Google Scholar 

  • Berg L. M., Pálsson S. and Lascoux M. (2001). Fitness and sexual response to population density in Daphnia pulex. Freshwater Biology 46: 667–677

    Article  Google Scholar 

  • Betancourt A. J. and Presgraves D. C. (2002). Linkage limits the power of natural selection in Drosophila. Proceedings of the National Academy of Sciences USA 99: 13616–13620

    Article  CAS  Google Scholar 

  • Boersma M. and Spaak P. (1999). Environmental stress and local adaptation in Daphnia magna. Limnology and Oceanography 44: 393–402

    Article  Google Scholar 

  • Boersma M. and Spaak P. (1998). Predator-mediated plasticity in morphology, life history and behavior of Daphnia: the uncoupling of responses. American Naturalist 152: 237–248

    Article  PubMed  CAS  Google Scholar 

  • Brewer M. C. (1998). Mating behaviours of Daphnia pulicaria, a cyclic parthenogen: comparisons with copepods. Philosophical Transactions of the Royal Society of London B 353: 805–815

    Article  Google Scholar 

  • Burns C. W. (1995). Effects of crowding and different food levels on growth and reproductive investment of Daphnia. Oecologia 101: 234–244

    Article  Google Scholar 

  • Cáceres C. E. and Tessier A. J. (2004). Incidence of diapause varies among populations of Daphnia pulicaria. Oecologia 141: 425–431

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Carvalho A. B., Sampaio M. C., Varandas F. R. and Klaczko L. B. (1998). An experimental demonstration of Fisher’s Principle: evolution of sexual proportion by natural selection. Genetics 148: 719–731

    PubMed  CAS  Google Scholar 

  • Carvalho G. R. and Hughes R. N. (1983). The effect of food availability, female culture-density and photoperiod on ephippia production in Daphnia magna Straus (Crustacea: Cladocera). Freshwater Biology 13: 37–46

    Article  Google Scholar 

  • Chadwick W. and Little T. J. (2005). A parasite-mediated life-history shift in Daphnia magna. Proceedings of the Royal Society of London B 272: 505–509

    Article  Google Scholar 

  • Cleuvers M., Goser B. and Ratte H.-T. (1997). Life-history shift by intraspecific interaction in Daphnia magna: change in reproduction from quantity to quality. Oecologia 110: 337–345

    Article  Google Scholar 

  • Crease T. J. and Hebert P. D. N. (1983). A test for the production of sexual pheromones by Daphnia magna (Crustacea: Cladocera). Freshwater Biology 13: 491–496

    Article  Google Scholar 

  • Declerck S. (2005). The study of biodiversity in freshwater habitats: societal relevance and suggestions for priorities in science policy. Hydrobiologia 542: 1–9

    Article  Google Scholar 

  • Vanoverbeke J. (1999). An uncoupling of male and sexual egg production leads to reduced inbreeding in the cyclical parthenogen Daphnia. Proceedings of the Royal Society of London B 266: 2471–2477

    Article  Google Scholar 

  • Deng H.-W. (1996). Environmental and genetic control of sexual reproduction in Daphnia. Heredity 76: 449–458

    Google Scholar 

  • Deng H.-W. (1997a). Increase in developmental instability upon inbreeding in Daphnia. Heredity 78: 182–189

    Article  Google Scholar 

  • Deng H.-W. (1997b). Photoperiodic response of sexual reproduction in the Daphnia pulex group is reversed in two distinct habitats. Limnology and Oceanography 42: 609–611

    Google Scholar 

  • Dudycha J. L. (2004). Mortality dynamics of Daphnia in contrasting habitats and their role in ecological divergence. Freshwater Biology 49: 505–514

    Article  Google Scholar 

  • (2000). Biological Test Method: Reference Method for Determining Acute Lethality of Effluents to Daphnia magna. Environmental Technology Centre, Ottawa

    Google Scholar 

  • Ferrari D. C. and Hebert P. D. N. (1982). The induction of sexual reproduction in Daphnia magna: genetic differences between arctic and temperate populations. Canadian Journal of Zoology 60: 2143–2148

    Article  Google Scholar 

  • Fisher R. A. (1930). The Genetical Theory of Natural Selection. Claredon Press, Oxford

    Google Scholar 

  • Fitzsimmons J. M. and Innes D. J. (2005). No evidence of Wolbachia among Great Lakes area populations of Daphnia pulex (Crustacea: Cladocera). Journal of Plankton Research 27: 121–124

    Article  Google Scholar 

  • Glazier D. S. (1992). Effects of food, genotype and maternal size and age on offspring investment in Daphnia magna. Ecology 73: 910–926

    Article  Google Scholar 

  • Gliwicz Z. M. and Guisande C. (1992). Family planning in Daphnia: resistance to starvation in offspring born to mothers grown at different food levels. Oecologia 91: 463–467

    Article  Google Scholar 

  • Gustafsson S., Rengefors K. and Hansson L.-A. (2005). Increased consumer fitness following transfer of toxin tolerance to offspring via maternal effects. Ecology 86: 2561–2567

    Google Scholar 

  • Hadany L. and Feldman M. W. (2005). Evolutionary traction: the cost of adaptation and the evolution of sex. Journal of Evolutionary Biology 18: 309–314

    Article  PubMed  CAS  Google Scholar 

  • Hebert P. D. N. (1987). Genotypic characteristics of the Cladocera. Hydrobiologia 145: 183–193

    Google Scholar 

  • Hebert P. D. N., Beaton M. J., Schwartz S. S. and Stanton D. J. (1989). Polyphyletic origins of asexuality in Daphnia pulex. I. breeding-system variation and levels of clonal diversity. Evolution 43: 1004–1015

    Article  Google Scholar 

  • Hebert P. D. N. and Crease T. (1983). Clonal diversity in populations of Daphnia pulex reproducing by obligate parthenogenesis. Heredity 51: 353–369

    Google Scholar 

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

    Article  Google Scholar 

  • Hurlbert S. H. (1984). Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54: 187–211

    Article  Google Scholar 

  • Innes D. J. (1989). Genetics of Daphnia obtusa: genetic load and linkage analysis in a cyclical parthenogen. Journal of Heredity 80: 6–10

    Google Scholar 

  • Innes D. J. (1997). Sexual reproduction of Daphnia pulex in a temporary habitat. Oecologia 111: 53–60

    Article  Google Scholar 

  • Innes D. J. and Dunbrack R. L. (1993). Sex allocation variation in␣Daphnia pulex. Journal of Evolutionary Biology 6: 559–575

    Article  Google Scholar 

  • Innes D. J., Fox C. J. and Winsor G. L. (2000). Avoiding the cost of males in obligately asexual Daphnia pulex (Leydig). Proceedings of the Royal Society of London B 267: 991–997

    Article  CAS  Google Scholar 

  • Innes D. J. and Hebert P. D. N. (1988). The origin and genetic basis of obligate parthenogenesis in Daphnia pulex. Evolution 42: 1024–1035

    Article  Google Scholar 

  • Innes D. J., Schwartz S. S. and Hebert P. D. N. (1986). Genotypic diversity and variation in mode of reproduction among populations in the Daphnia pulex group. Heredity 57: 345–355

    Google Scholar 

  • Innes D. J. and Singleton D. R. (1994). Variation in reproduction and sex allocation among clones of Daphnia pulex. In: Beaumont, A. R. (eds) Genetics and Evolution of Aquatic Organisms, pp 335–342. Chapman and Hall, London

    Google Scholar 

  • Innes D. J. and Singleton D. R. (2000). Variation in allocation to sexual and asexual reproduction among clones of cyclically parthenogenetic Daphnia pulex (Crustacea: Cladocera). Biological Journal of the Linnean Society 71: 771–787

    Article  Google Scholar 

  • Kerfoot W. C. and Weider L. J. (2004). Experimental paleoecology (resurrection ecology): chasing Van Valen’s Red Queen hypothesis. Limnology and Oceanography 49: 1300–1316

    Article  Google Scholar 

  • Kessler K. and Lampert W. (2004). Fitness optimization of Daphnia in a trade-off between food and temperature. Oecologia 140: 381–387

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Korpelainen H. (1986). The effects of temperature and photoperiod on life history parameters of Daphnia magna (Crustacea: Cladocera). Freshwater Biology 16: 615–620

    Article  Google Scholar 

  • Korpelainen H. (1992). Lowered female reproductive effort as an indicator for increased male production and sexuality in Daphnia (Crustacea: Cladocera). Invertebrate Reproduction and Development 22: 281–290

    Google Scholar 

  • LaMontagne J. M. and McCauley E. (2001). Maternal effects in Daphnia: what mothers are telling their offspring and do they listen?. Ecology Letters 4: 64–71

    Article  Google Scholar 

  • Larsson P. (1991). Intraspecific variability in response to stimuli for male and ephippia formation in Daphnia pulex. Hydrobiologia 225: 281–290

    Article  Google Scholar 

  • Lass S. and Bittner K. (2002). Facing multiple enemies: parasitised hosts respond to predator kairomones. Oecologia 132: 344–349

    Article  Google Scholar 

  • Loaring J. M. and Hebert P. D. N. (1981). Ecological differences among clones of Daphnia pulex Leydig. Oecologia 51: 162–168

    Article  Google Scholar 

  • López S. and Domínguez C. A. (2003). Sex choice in plants: facultative adjustment of the sex ratio in the perennial herb Begonia gracilis. Journal of Evolutionary Biology 16: 1177–1185

    Article  PubMed  Google Scholar 

  • Lürling M., Roozen F. and Goser B. (2003). Response of Daphnia to substances released from crowded congeners and conspecifics. Journal of Plankton Research 25: 967–978

    Article  Google Scholar 

  • Lushai G., Loxdale H. D. and Allen J. A. (2003). The dynamic clonal genome and its adaptive potential. Biological Journal of the Linnean Society 79: 193–208

    Article  Google Scholar 

  • Lynch M., Spitze K. and Crease T. (1989). The distribution of life-history variation in the Daphnia pulex complex. Evolution 43: 1724–1736

    Article  Google Scholar 

  • Lynch M., Weider L. J. and Lampert W. (1986). Measurement of the carbon balance in Daphnia. Limnology and Oceanography 31: 17–33

    Article  Google Scholar 

  • Mikulski A., Czernik M. and Pijanowska J. (2005). Induction time and reversibility of changes in Daphnia life history caused by the presence of fish. Journal of Plankton Research 27: 757–762

    Article  Google Scholar 

  • Mitchell S. E. and Read A. F. (2005). Poor maternal environment enhances offspring disease resistance in an invertebrate. Proceedings of the Royal Society of London B 272: 2601–2607

    Article  Google Scholar 

  • Mitchell S. E., Read A. F. and Little T. J. (2004). The effect of a pathogen epidemic on the genetic structure and reproductive strategy of the crustacean Daphnia magna. Ecology Letters 7: 848–858

    Article  Google Scholar 

  • Mitchell S. E., Rogers E. S., Little T. J. and Read A. F. (2005). Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59: 70–80

    Article  PubMed  Google Scholar 

  • Mu X. and LeBlanc G. A. (2002). Environmental antiecdysteroids alter embryo development in the crustacean Daphnia magna. Journal of Experimental Zoology 292: 287–292

    Article  PubMed  CAS  Google Scholar 

  • Nelson W. A., McCauley E. and Wrona F. J. (2005). Stage-structured cycles promote genetic diversity in a predator-prey system of Daphnia and algae. Nature 433: 413–417

    Article  PubMed  CAS  Google Scholar 

  • (1998). OECD Guidelines for Testing of Chemicals: Daphnia magna Reproduction Test. Organisation for Economic Co-operation and Development, Paris

    Google Scholar 

  • Olmstead A. W. and LeBlanc G. A. (2001). Temporal and quantitative changes in sexual reproductive cycling of the cladoceran Daphnia magna by a juvenile hormone analog. Journal of Experimental Zoology 290: 148–155

    Article  PubMed  CAS  Google Scholar 

  • Olmstead A. W. and LeBlanc G. A. (2002). Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna. Journal of Experimental Zoology 293: 736–739

    Article  PubMed  CAS  Google Scholar 

  • Paland S., Colbourne J. K. and Lynch M. (2005). Evolutionary history of contagious asexuality in Daphnia pulex. Evolution 59: 800–813

    Article  PubMed  CAS  Google Scholar 

  • Peer K. and Taborsky M. (2004). Female ambrosia beetles adjust their offspring sex ratio according to outbreeding opportunities for their sons. Journal of Evolutionary Biology 17: 257–264

    Article  PubMed  CAS  Google Scholar 

  • Pijanowska J. and Kowalczewski A. (1997). Cues from injured Daphnia and from cyclopoids feeding on Daphnia can modify life histories of conspecifics. Hydrobiologia 350: 99–103

    Article  Google Scholar 

  • Printes L. B. and Callaghan A. (2003). Intraclonal variability in Daphnia acetylcholinesterase activity: the implications for its applicability as a biomarker. Environmental Toxicology and Chemistry 22: 2042–2047

    Article  PubMed  CAS  Google Scholar 

  • Rice W. R. and Chippindale A. K. (2001). Sexual recombination and the power of selection. Science 294: 555–559

    Article  PubMed  CAS  Google Scholar 

  • Ruvinsky A. O., Perelygin A. A., Lobkov Y. I. and Belyaev D. K. (1986). Factors organising and maintaining polymorphism in a cyclic parthenogenetic species: Daphnia pulex. Heredity 57: 15–22

    Google Scholar 

  • Salathé P. and Ebert D. (2003). The effects of parasitism and inbreeding on the competitive ability in Daphnia magna: evidence for synergistic epistasis. Journal of Evolutionary Biology 16: 976–985

    Article  PubMed  Google Scholar 

  • Sanders R. W., Williamson C. E., Stutzman P. L., Moeller R. E., Goulden C. E. and Aoki-Goldsmith R. (1996). Reproductive success of “herbivorous” zooplankton fed algal and nonalgal food resources. Limnology and Oceanography 41: 1295–1305

    Google Scholar 

  • Sarre S. D., Georges A. and Quinn A. (2004). The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. BioEssays 26: 639–645

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Simon J.-C., Delmotte F., Rispe C. and Crease T. (2003). Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biological Journal of the Linnean Society 79: 151–163

    Article  Google Scholar 

  • Simon J.-C., Rispe C. and Sunnucks P. (2002). Ecology and evolution of sex in aphids. Trends in Ecology and Evolution 17: 34–39

    Article  Google Scholar 

  • Ślusarczyk M. (1995). Predator-induced diapause in Daphnia. Ecology 76: 1008–1013

    Article  Google Scholar 

  • Spaak P., Denk A., Boersma M. and Weider L. J. (2004). Spatial and temporal patterns of sexual reproduction in a hybrid Daphnia species complex. Journal of Plankton Research 26: 625–635

    Article  Google Scholar 

  • Stabell O. B., Ogbebo F. and Primicerio R. (2003). Inducible defences in Daphnia depend on latent alarm signals from conspecific prey activated in predators. Chemical Senses 28: 141–153

    Article  PubMed  CAS  Google Scholar 

  • Stross R. G. (1969). Photoperiod control of diapause in Daphnia. III. Two-stimulus control of long-day, short-day induction. Biological Bulletin 137: 359–374

    Google Scholar 

  • Tessier A. J. and Cáceres C. E. (2004). Differentiation in sex investment by clones and populations of Daphnia. Ecology Letters 7: 695–703

    Article  Google Scholar 

  • Trivers R. L. and Willard D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science 179: 90–92

    PubMed  CAS  Google Scholar 

  • (2002). Methods for Measuring the Acute Toxicity of Effluents and Receiving Waters to Freshwater and Marine Organisms. U.S. Environmental Protection Agency, Washington

    Google Scholar 

  • Valenzuela N., Adams D. C. and Janzen F. J. (2003). Pattern does not equal process: exactly when is sex environmentally determined?. American Naturalist 161: 676–683

    Article  PubMed  Google Scholar 

  • Vrijenhoek R. C. (1998). Animal clones and diversity: are natural clones generalists or specialists?. BioScience 48: 617–628

    Article  Google Scholar 

  • Weber A. and Declerck S. (1997). Phenotypic plasticity of Daphnia life history traits in response to predator kairomones: genetic variability and evolutionary potential. Hydrobiologia 360: 89–99

    Article  Google Scholar 

  • Weetman D. and Atkinson D. (2002). Antipredator reaction norms for life history traits in Daphnia pulex: dependence on temperature and food. Oikos 98: 299–307

    Article  Google Scholar 

  • Weinzierl R. P., Schmidt P. and Michiels N. K. (1999). High fecundity and low fertility in parthenogenetic planarians. Invertebrate Biology 118: 87–94

    Article  Google Scholar 

  • Whittingham L. A., Dunn P. O. and Nooker J. K. (2005). Maternal influences on brood sex ratios: an experimental study in tree swallows. Proceedings of the Royal Society of London B 272: 1775–1780

    Article  Google Scholar 

  • Winsor G. L. and Innes D. J. (2002). Sexual reproduction in Daphnia pulex (Crustacea: Cladocera): observations on male mating behaviour and avoidance of inbreeding. Freshwater Biology 47: 441–450

    Article  Google Scholar 

  • Yampolsky L. Y. (1992). Genetic variation in the sexual reproduction rate within a population of a cyclic parthenogen, Daphnia magna. Evolution 46: 833–837

    Article  Google Scholar 

  • Yasumoto K., Nishigami A., Yasumoto M., Kasai F., Okada Y., Kusumi T. and Ooi T. (2005). Aliphatic sulfates released from Daphnia induce morphological defense of phytoplankton: isolation and synthesis of kairomones. Tetrahedron Letters 46: 4765–4767

    Article  CAS  Google Scholar 

  • Zhang L. and Baer K. N. (2000). The influence of feeding, photoperiod and selected solvents on the reproductive strategies of the water flea, Daphnia magna. Environmental Pollution 110: 425–430

    Article  PubMed  CAS  Google Scholar 

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Fitzsimmons, J.M., Innes, D.J. Inter-genotype variation in reproductive response to crowding among Daphnia pulex . Hydrobiologia 568, 187–205 (2006). https://doi.org/10.1007/s10750-006-0104-5

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