Cite this paper:
LI Wenjie, NIU Cuijuan, LI Xiaoxuan. Offspring of aged mothers of rotifer Brachionus calyciflorus shows lower sexual propensity than their elder siblings under crowded conditions[J]. Journal of Oceanology and Limnology, 2019, 37(5): 1604-1610

Offspring of aged mothers of rotifer Brachionus calyciflorus shows lower sexual propensity than their elder siblings under crowded conditions

LI Wenjie, NIU Cuijuan, LI Xiaoxuan
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875, China
Abstract:
Maternal effects are one of the most interesting topics in evolutionary ecology as they can affect the rate of evolution and population dynamics by phenotypic manipulation of offspring related to fitness. At present, studies examining the interaction between maternal environment effects and maternal age (birth order) effects are scarce. We designed an experiment to reveal whether environmentally induced maternal manipulation works equally on offspring across birth orders in rotifer Brachionus calyciflorus. In the experiment, newborn amictic mothers (F0) were cultured parallelly in low (LD) and high (HD) population density. Offspring (F1) of young (YF0) and old (OF0) mothers in both LD and HD groups were cultured under a crowded condition and the mixis ratios of both F1 and F2 were examined. Results show that F1 from HD-YF0 had a significantly higher mixis ratio and those amictic ones produced daughters (F2) with higher mixis ratio in response to crowding than those from HD-OF0. In contrast, no such differences among F1 siblings were found in the LD-F0 group. Therefore, the effect of maternal age on the sexual propensity of the offspring can be affected independently by the maternal population density.
Key words:    rotifer|Brachionus calyciflorus|sexual propensity|birth order effect|maternal environment|mixis ratio   
Received: 2018-07-30   Revised: 2018-10-11
Tools
PDF (443 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by LI Wenjie
Articles by NIU Cuijuan
Articles by LI Xiaoxuan
References:
Alekseev V, Lampert W. 2004. Maternal effects of photoperiod and food level on life history characteristics of the Cladoceran Daphnia Pulicaria Forbes. Hydrobilogia, 526(1):225-230, https://doi.org/10.1023/B:HYDR.0000041600.16226.12.
Berkeley S A, Chapman C, Sogard S M. 2004. Maternal age as a determinant of larval growth and survival in a marine fish, Sebastes melanops. Ecology, 85(5):1 258-1 264, https://doi.org/10.1890/03-0706.
Bernardo J. 1996. The particular maternal effect of propagule size, especially egg size:patterns, models, quality of evidence and interpretations. Integr. Comp. Biol., 36(2):216-236, https://doi.org/10.1093/icb/36.2.216.
Carmona M J, Serra M, Miracle M R. 1993. Relationships between mixis in Brachionus plicatilis and preconditioning of culture medium by crowding. Hydrobiologia, 255-256(1):145-152, https://doi.org/10.1007/BF00025832.
Dantzer B, Newman A E M, Boonstra R, Palme R, Boutin S, Humphries M M, McAdam A G. 2013. Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science, 340(6137):1 215-1 217, https://doi.org/10.1126/science.1235765.
FACHB-2016 (Freshwater Algae Culture Collection of the Institute of Hydrobiology). 2016. SE (Brostol's solution)medium. http://algae.ihb.ac.cn/Products/ProductDetail.aspx?product=3.
Fox C W. 1993. The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculatus (Coleoptera:Bruchidae).Oecologia, 96(1):139-146, https://doi.org/10.1007/BF00318042.
Fussmann G F, Ellner S P, Hairston N G. 2003. Evolution as a critical component of plankton dynamics. Proc. Roy. Soc.B Biol. Sci., 270(1519):1 015-1 022, https://doi.org/10.1098/rspb.2003.2335.
Fussmann G F, Kramer G, Labib M. 2007. Incomplete induction of mixis in Brachionus calyciflorus:patterns of reproduction at the individual level. Hydrobiologia, 593(1):111-119, https://doi.org/10.1007/s10750-007-9041-1.
Gilbert J J, McPeek M A. 2013. Maternal age and spine development in a rotifer:ecological implications and evolution. Ecology, 94(10):2 166-2 172, https://doi.org/10.1890/13-0768.1.
Gilbert J J, Schröder T. 2007. Intraclonal variation in propensity for mixis in several rotifers:variation among females and with maternal age. Hydrobiologia, 593(1):121-128, https://doi.org/10.1007/s10750-007-9040-2.
Gilbert J J. 1974. Dormancy in rotifers. Trans. Am. Microsc.Soc., 93(4):490-513, https://doi.org/10.2307/3225154.
Gilbert J J. 2002. Endogenous regulation of environmentally induced sexuality in a rotifer:a multigenerational parental effect induced by fertilisation. Freshw. Biol., 47(9):1 633-1 641, https://doi.org/10.1046/j.1365-2427.2002.00900.x.
Gilbert J J. 2003. Environmental and endogenous control of sexuality in a rotifer life cycle:developmental and population biology. Evol. Dev., 5(1):19-24, https://doi.org/10.1046/j.1525-142X.2003.03004.x.
Gilbert J J. 2004. Population density, sexual reproduction and diapause in monogonont rotifers:new data for Brachionus and a review. J. Limnol., 63(1S):32-36, https://doi.org/10.4081/jlimnol.2004.s1.32.
Gilbert J J. 2007. Induction of mictic females in the rotifer Brachionus:oocytes of amictic females respond individually to population-density signal only during oogenesis shortly before oviposition. Freshw. Biol., 52(8):1 417-1 426, https://doi.org/10.1111/j.1365-2427.2007.01782.x.
Gillespie D O S, Russell A F, Lummaa V. 2013. The effect of maternal age and reproductive history on offspring survival and lifetime reproduction in preindustrial humans. Evolution, 67(7):1 964-1 974, https://doi.org/10.1111/evo.12078.
Hercus M J, Hoffmann A A. 2000. Maternal and grandmaternal age influence offspring fitness in Drosophila. Proc. Roy.Soc. B Biol. Sci., 267(1457):2 105-2 110, https://doi.org/10.1098/rspb.2000.1256.
JoséCarmona M, Serra M, Miracle M R. 1994. Effect of population density and genotype on life-history traits in the rotifer Brachionus plicatilis O.F. Müller. J. Exp. Mar.Biol.Ecol.,182(2):223-235, https://doi.org/10.1016/0022-0981(94)90053-1.
Kern S, Ackermann M, Stearns S C, Kawecki T J. 2001. Decline in offspring viability as a manifestation of aging in Drosophila melanogaster. Evolution, 55(9):1 822-1 831, https://doi.org/10.1111/j.0014-3820.2001.tb00831.x.
Kilham S S, Kreeger D A, Lynn S G, Goulden C E, Herrera L. 1998. COMBO:a defined freshwater culture medium for algae and zooplankton. Hydrobiologia, 377(1-3):147-159, https://doi.org/10.1023/A:1003231628456.
Kuijper B, Hoyle R B. 2015. When to rely on maternal effects and when on phenotypic plasticity? Evolution, 69(4):950-968, https://doi.org/10.1111/evo.12635.
Lansing A I. 1947. A transmissible, cumulative, and reversible factor in aging. J. Gerontol., 2(3):228-239, https://doi.org/10.1093/geronj/2.3.228.
Lints F A, Hoste C. 1977. The Lansing effect revisited. Ⅱ-Cumulative and spontaneously reversible parental age effects on fecundity in Drosophila melanogaster. Evolution, 31(2):387-404, https://doi.org/10.1111/j.1558-5646.1977.tb01020.x.
Mcintyre G S, Gooding R H. 2000. Effects of maternal age on larval competitiveness in house flies. Heredity, 85(5):480-489, https://doi.org/10.1046/j.1365-2540.2000.00787.x.
Mousseau T A, Fox C W. 1998. The adaptive significance of maternal effects. Trends Ecol. Evol., 13(10):403-407, https://doi.org/10.1016/S0169-5347(98)01472-4.
Opit G P, Throne J E. 2007. Influence of maternal age on the fitness of progeny in the rice weevil, Sitophilus oryzae(Coleoptera:Curculionidae). Environ. Entomol., 36(1):83-89, https://doi.org/10.1603/0046-225X(2007)36[83:IOMAOT]2.0.CO;2.
Plaistow S J, Shirley C, Collin H, Cornell S J, Harney E D. 2015. Offspring provisioning explains clone-specific maternal age effects on life history and life span in the water flea, Daphnia pulex. Am. Nat., 186(3):376-389, https://doi.org/10.1086/682277.
Raveh S, Vogt D, Kölliker M. 2016. Maternal programming of offspring in relation to food availability in an insect (Forficula auricularia). Proc. Roy. Soc. B Biol. Sci., 283(1828):20152936, https://doi.org/10.1098/rspb.2015.2936.
Rougier C, Pourriot R. 1977. Aging and control of the reproduction in Brachionus calyciflorus (Pallas)(Rotatoria). Exp. Gerontol., 12(3-4):137-151, https://doi.org/10.1016/0531-5565(77)90022-5.
Schröder T. 2005. Diapause in monogonont rotifers.Hydrobiologia, 546(1):291-306, https://doi.org/10.1007/s10750-005-4235-x.
Serra M, Snell T W, King C E. 2004. The timing of sex in cyclically parthenogenetic rotifers. In:Moya A, Font E eds. Evolution:From Molecules to Ecosystems. Oxford University Press, Oxford. p.135-146.
Snell T W, Boyer E M. 1988. Thresholds for mictic female production in the rotifer Brachionus plicatilis (Muller). J.Exp. Mar. Biol. Ecol., 124(2):73-85, https://doi.org/10.1016/0022-0981(88)90112-8.
Snell T W, Kubanek J, Carter W, Payne A B, Kim J, Hicks M K, Stelzer C P. 2006. A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Mar.Biol., 149(4):763-773, https://doi.org/10.1007/s00227-006-0251-2.
Snell T W. 1998. Chemical ecology of rotifers. Hydrobiologia, 387-388(0):267-276, https://doi.org/10.1023/A:1017087003334.
Stelzer C P, Snell T W. 2003. Induction of sexual reproduction in Brachionus plicatilis (Monogononta, Rotifera) by a density-dependent chemical cue. Limnol. Oceanogr., 48(2):939-943, https://doi.org/10.4319/lo.2003.48.2.0939.
Stelzer C P. 2011. The cost of sex and competition between cyclical and obligate parthenogenetic rotifers. Am. Nat., 177(2):E43-E53, https://doi.org/10.1086/657685.
Storm J J, Lima S L. 2010. Mothers forewarn offspring about predators:a transgenerational maternal effect on behavior.Am.Nat.,175(3):382-390, https://doi.org/10.1086/650443.
Sun D, Niu C J. 2012. Maternal crowding can enhance the propensity of offspring to produce mictic females in the rotifer Brachionus calyciflorus. J. Plankton Res., 34(8):732-737, https://doi.org/10.1093/plankt/fbs044.
Tollrian R. 1995. Predator-induced morphological defenses:costs, life history shifts, and maternal effects in Daphnia pulex. Ecology, 76(6):1 691-1 705, https://doi.org/10.2307/1940703.
Uller T, English S, Pen I. 2015. When is incomplete epigenetic resetting in germ cells favoured by natural selection?Proc. Roy. Soc. B Biol. Sci., 282(1811):20150682, https://doi.org/10.1098/rspb.2015.0682.
Uller T, Nakagawa S, English S. 2013. Weak evidence for anticipatory parental effects in plants and animals. J. Evol.Biol., 26(10):2 161-2 170, https://doi.org/10.1111/jeb.12212.
Uller T. 2008. Developmental plasticity and the evolution of parental effects. Trends Ecol. Evol., 23(8):432-438, https://doi.org/10.1016/j.tree.2008.04.005.
Yin X W, Zhao N X, Wang B H, Li W J, Zhang Z N. 2015.Transgenerational and within-generational induction of defensive morphology in Brachionus calyciflorus(rotifera):importance of maternal effect. Hydrobiologia, 742(1):313-325, https://doi.org/10.1007/s10750-014-1995-1.
Copyright © Haiyang Xuebao