Environmental stability via sexual reproduction of cyclical parthenogenetic rotifers affects offspring’s population performances: maternal effects on population dynamics

Huanhuan XU; Yingying GE; Kangning LIU; Cuijuan NIU

doi:10.1007/s00343-025-4268-0

Your Location：

Home >

Browse articles >

Environmental stability via sexual reproduction of cyclical parthenogenetic rotifers affects offspring’s population performances: maternal effects on population dynamics

Ecology | Updated：2025-12-16

- Environmental stability via sexual reproduction of cyclical parthenogenetic rotifers affects offspring’s population performances: maternal effects on population dynamics
- Environmental stability via sexual reproduction of cyclical parthenogenetic rotifers affects offspring’s population performances: maternal effects on population dynamics
- 海洋湖沼学报(英文) 2025年43卷第6期页码：1892-1901
- Affiliations：
  
  1.MOE Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875, China
  2.College of Fisheries, Henan Normal University, Xinxiang 453007, China
  3.Observation and Research Station on Water Ecosystem in Danjiangkou Reservoir of Henan Province, Nanyang 474450, China
- Author bio：
  
  cjniu@bnu.edu.cn
- Funds：
  
  the National Natural Science Foundation of China(32071528)
- DOI：10.1007/s00343-025-4268-0
  中图分类号：
- 收稿：2024-10-15，
  
  网络首发：2025-02-14，
  
  纸质出版：2025-11-01
- Accepted：
Scan QR Code
Huanhuan XU, Yingying GE, Kangning LIU, 等. Environmental stability via sexual reproduction of cyclical parthenogenetic rotifers affects offspring’s population performances: maternal effects on population dynamics[J]. 海洋湖沼学报(英文), 2025,43(6):1892-1901.

XU Huanhuan,GE Yingying,LIU Kangning,et al.Environmental stability via sexual reproduction of cyclical parthenogenetic rotifers affects offspring’s population performances: maternal effects on population dynamics[J].Journal of Oceanology and Limnology,2025,43(06):1892-1901.
Huanhuan XU, Yingying GE, Kangning LIU, 等. Environmental stability via sexual reproduction of cyclical parthenogenetic rotifers affects offspring’s population performances: maternal effects on population dynamics[J]. 海洋湖沼学报(英文), 2025,43(6):1892-1901. DOI： 10.1007/s00343-025-4268-0.

XU Huanhuan,GE Yingying,LIU Kangning,et al.Environmental stability via sexual reproduction of cyclical parthenogenetic rotifers affects offspring’s population performances: maternal effects on population dynamics[J].Journal of Oceanology and Limnology,2025,43(06):1892-1901. DOI： 10.1007/s00343-025-4268-0.

摘要

Abstract

Environmental fluctuations are a pervasive natural phenomenon that typically favor diverse maternal investment strategies. Organisms across various evolutionary lineages have acquired the ability to enter the dormancy state to tolerate conditions that are unsuitable for normal life activities. In cyclical parthenogenesis

sexual reproduction is generally linked with dormancy

thereby enhancing the long-term fitness of populations through positive feedback mechanisms. This study evaluates the impact of environmental variability on offspring population dynamics through sexual reproduction in the rotifer

Brachionus

calyciflorus

. We found that mictic females (sexual females) exposed to low-predictability environments produced resting eggs with a sporadic hatching pattern

reduced hatching rate

and smaller sizes of resting egg

embryo

and stem females

while increasing variations in fertilization among individuals to maximize population fitness. Variations in population growth could be manifested in enhanced reproductive capacity 2–3 d post-hatching

along with differences in fecundity among individuals. This suggests that dormant eggs from unstable environments may prioritize offspring survival and adjust to increased fertilization among individuals. This adaptive strategy enables rotifer populations to rapidly adjust to environmental changes

thus avoiding extinction and thriving in diverse habitats. Our systematic study enhances the understanding of how environmental stability affects long-term population fitness in cyclical parthenogens.

关键词

Keywords

references

Barbosa M , Lopes I , Venâncio C et al . 2015 . Maternal response to environmental unpredictability . Ecol. Evol. , 5 ( 20 ): 4567 - 4577 , https://doi.org/10.1002/ece3.1723 https://doi.org/10.1002/ece3.1723 .

Bischof R , Milleret C , Dupont P et al . 2020 . Estimating and forecasting spatial population dynamics of apex predators using transnational genetic monitoring. P . Natl . Acad . Sci . USA , 117 ( 48 ): 30531 - 30538 , https://doi.org/10.1073/pnas.2011383117 https://doi.org/10.1073/pnas.2011383117 .

Brendonck L , De Meester L . 2003 . Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment . Hydrobiologia , 491 ( 1 ): 65 - 84 , https://doi.org/10.1023/A:1024454905119 https://doi.org/10.1023/A:1024454905119 .

Bronikowski A M , Clark M E , Rodd F H et al . 2002 . Population-dynamic consequences of predator-induced life history variation in the guppy ( Poecilia reticulata ) . Ecology , 83 ( 8 ): 2194 - 2204 , https://doi.org/10.1890/0012-9658(2002)083 https://doi.org/10.1890/0012-9658(2002)083 [2194:pdcopi ] 2.0.co; 2 .

Clegg J S . 2001 . Cryptobiosis-a peculiar state of biological organization. Comp . Biochem . Phys . B , 128 ( 4 ): 613 - 624 , https://doi.org/10.1016/S1096-4959(01)00300-1 https://doi.org/10.1016/S1096-4959(01)00300-1 .

de Stasio B T . 2004 . Diapause in Calanoid Copepods: within-clutch hatching patterns . J. Limnol. , 63 ( S1 ): 26 - 31 , https://doi.org/10.4081/jlimnol.2004.s1.26 https://doi.org/10.4081/jlimnol.2004.s1.26 .

FACHB-2016 . Freshwater Algae Culture Collection of the Institute of Hydrobiology . SE (Brostol's Solution) Medium. http://algae.ihb.ac.cn/Products/ProductDetail.aspx?product=3 http://algae.ihb.ac.cn/Products/ProductDetail.aspx?product=3 . (in Chinese)

García-Roger E M , Carmona M J , Serra M . 2006 . A simple model relating habitat features to a diapause egg bank . Limnol. Oceanogr. , 51 ( 3 ): 1542 - 1547 , https://doi.org/10.4319/lo.2006.51.3.1542 https://doi.org/10.4319/lo.2006.51.3.1542 .

García-Roger E M , Ortells R . 2018 . Trade-offs in rotifer diapausing egg traits: survival, hatching, and lipid content . Hydrobiologia , 805 ( 1 ): 339 - 350 , https://doi.org/10.1007/s10750-017-3317-x https://doi.org/10.1007/s10750-017-3317-x .

García-Roger E M , Serra M , Carmona M J . 2014 . Bet-hedging in diapausing egg hatching of temporary rotifer populations-A review of models and new insights . Int. Rev. Hydrobiol. , 99 ( 1-2 ): 96 - 106 , https://doi.org/10.1002/iroh.201301708 https://doi.org/10.1002/iroh.201301708 .

Gilbert J J . 2017 . Resting-egg hatching and early population development in rotifers: a review and a hypothesis for differences between shallow and deep waters . Hydrobiologia , 796 ( 1 ): 235 - 243 , https://doi.org/10.1007/s10750-016-2867-7 https://doi.org/10.1007/s10750-016-2867-7 .

Gilbert J J , Schröder T . 2004 . Rotifers from diapausing, fertilized eggs: unique features and emergence. Limnol . Oceanogr ., 49 (4part 2 ): 1341 - 1354 , https://doi.org/10.4319/lo.2004.49.4_part_2.1341 https://doi.org/10.4319/lo.2004.49.4_part_2.1341 .

Hagiwara A , Kadota Y , Hino A . 2005 . Maternal effect by stem females in Brachionus plicatilis : effect of starvation on mixis induction in offspring . Hydrobiologia , 546 ( 1 ): 275 - 279 , https://doi.org/10.1007/1-4020-4408-9_28 https://doi.org/10.1007/1-4020-4408-9_28 .

Hansen B W . 2019 . Copepod embryonic dormancy: "an egg is not just an egg" . The Biological Bulletin , 237 ( 2 ): 145 - 169 , https://doi.org/10.1086/705546 https://doi.org/10.1086/705546 .

Hashimshony T , Levin L , Fröbius A C et al . 2024 . A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they "animal seeds"? BMC Genomics , 25 ( 1 ): 119 , https://doi.org/10.1186/s12864-024-09961-1 https://doi.org/10.1186/s12864-024-09961-1 .

Hu K , Xi Y L , Wang J X . 2010 . Life history characteristics of rotifer Brachionus calyciflorus from two lakes situated in different geographic regions . J. Lake Sci. , 22 ( 4 ): 585 - 590 , https://doi.org/10.1080/09500340.2010.529951. https://doi.org/10.1080/09500340.2010.529951. (in Chinese with English abstract)

Kilham S S , Kreeger D A , Lynn S G et al . 1998 . COMBO: a defined freshwater culture medium for algae and zooplankton . Hydrobiologia , 377 ( 1 ): 147 - 159 , https://doi.org/10.1023/A:1003231628456 https://doi.org/10.1023/A:1003231628456 .

Li W J , Niu C J , Bian S J . 2022 . Sex ratio in the mother's environment affects offspring population dynamics: maternal effects on population regulation. Proc . Royal Soc . B , 289 ( 1970 ): 20212530 , https://doi.org/10.1098/rspb.2021.2530 https://doi.org/10.1098/rspb.2021.2530 .

Li X X , Niu C J . 2018 . Maternal effects via resting eggs in predator defense of the rotifer Brachionus calyciflorus . Zool. Sci. , 35 ( 1 ): 49 - 56 , https://doi.org/10.2108/zs170062 https://doi.org/10.2108/zs170062 .

Lubzens E , Hamo R , Blais I et al . 2020 . Rotifer resting eggs: An alternative for rotifer mass cultures in fish farms-Lessons from a comprehensive study on production, storage and hatching of resting eggs . Aquaculture , 528 ( 2020 ): 735505 , https://doi.org/10.1016/j.aquaculture.2020.735505 https://doi.org/10.1016/j.aquaculture.2020.735505 .

Lundemo S , Falahati-Anbaran M , Stenøien H K . 2009 . Seed banks cause elevated generation times and effective population sizes of Arabidopsis thaliana in northern Europe . Mol. Ecol. , 18 ( 13 ): 2798 - 2811 , https://doi.org/10.1111/j.1365-294X.2009.04236.x https://doi.org/10.1111/j.1365-294X.2009.04236.x .

Mau T D , Quang-Hung D . 2023 . Effects of cultural conditions on life history characteristics of the freshwater rotifer Brachionus calyciflorus . Int . J . Aquat . Biol. , 11 ( 2 ): 104 - 114 , https://www.magiran.com/p2583539 https://www.magiran.com/p2583539 .

Moore M P , Whiteman H H , Martin R A . 2019 . A mother's legacy: the strength of maternal effects in animal populations . Ecol. Lett. , 22 ( 10 ): 1620 - 1628 , https://doi.org/10.1111/ele.13351 https://doi.org/10.1111/ele.13351 .

Pinceel T , Vanschoenwinkel B , Hawinkel W et al . 2017 . Aridity promotes bet hedging via delayed hatching: a case study with two temporary pond crustaceans along a latitudinal gradient . Oecologia , 184 ( 1 ): 161 - 170 , https://doi.org/10.1007/s00442-017-3858-8 https://doi.org/10.1007/s00442-017-3858-8 .

Pourriot R , Snell T W . 1983 . Resting eggs in rotifers . Hydrobiologia , 104 ( 1 ): 213 - 224 , https://doi.org/10.1007/BF00045970 https://doi.org/10.1007/BF00045970 .

Reed T E , Waples R S , Schindler D E et al . 2010 . Phenotypic plasticity and population viability: the importance of environmental predictability. P . Roy . Soc . B - Biol . Sci. , 277 ( 1699 ): 3391 - 3400 , https://doi.org/10.1098/rspb.2010.0771 https://doi.org/10.1098/rspb.2010.0771 .

Ricc C , Perletti F . 2006 . Starve and survive: stress tolerance and life-history traits of a bdelloid rotifer . Funct. Ecol. , 20 ( 2 ): 340 - 346 , https://doi.org/10.1111/j.1365-2435.2006.01082.x https://doi.org/10.1111/j.1365-2435.2006.01082.x .

Ripa J , Olofsson H , Jonzén N . 2010 . What is bet-hedging, really? P . Roy . Soc - B : Biol . Sci. , 277 ( 1685 ): 1153 - 1154 , https://doi.org/10.1098/rspb.2009.2023 https://doi.org/10.1098/rspb.2009.2023 .

Sarma S S S , Rao T R . 1987 . Effect of food level on body size and egg size in a growing population of the rotifer Brachionus patulus MULLER . Archiv für Hydrobiologie , 111 ( 2 ): 245 - 253 , https://doi.org/10.1127/archiv-hydrobiol/111/1987/245 https://doi.org/10.1127/archiv-hydrobiol/111/1987/245 .

Schröder T . 2005 . Diapause in monogonont rotifers . In: Herzig A, Gulati R D, Jersabek C D et al. eds . Rotifera X : Rotifer Research: Trends, New Tools and Recent Advances. Springer, Dordrecht. p . 291 - 306 , https://doi.org/10.1007/1-4020-4408-9_30 https://doi.org/10.1007/1-4020-4408-9_30 .

Serra M , Aparici E , Carmona M J . 2008 . When to be sexual: sex allocation theory and population density-dependent induction of sex in cyclical parthenogens . J. Plankton Res. , 30 ( 11 ): 1207 - 1214 , https://doi.org/10.1093/plankt/fbn077 https://doi.org/10.1093/plankt/fbn077 .

Serra M , Galiana A , Gómez A . 1997 . Speciation in monogonont rotifers . Hydrobiologia , 358 ( 1 ): 63 - 70 , https://doi.org/10.1023/A:1003155617297 https://doi.org/10.1023/A:1003155617297 .

Sheriff M J , Love O P . 2013 . Determining the adaptive potential of maternal stress . Ecol. Lett. , 16 ( 2 ): 271 - 280 , https://doi.org/10.1111/ele.12042 https://doi.org/10.1111/ele.12042 .

Simons A M . 2011 . Modes of response to environmental change and the elusive empirical evidence for bet hedging. P . Roy . Soc-B : Biol Sci. , 278 ( 1712 ): 1601 - 1609 , https://doi.org/10.1098/rspb.2011.0176 https://doi.org/10.1098/rspb.2011.0176 .

Sloat M R , Reeves G H . 2014 . Demographic and phenotypic responses of juvenile steelhead trout to spatial predictability of food resources . Ecology , 95 ( 9 ): 2423 - 2433 , https://doi.org/10.1890/13-1442.1 https://doi.org/10.1890/13-1442.1 .

Snell T W , Janssen C R . 1995 . Rotifers in ecotoxicology: a review . Hydrobiologia , 313 ( 1 ): 231 - 247 , https://doi.org/10.1007/BF00025956 https://doi.org/10.1007/BF00025956 .

Storey K B , Storey J M . 2012 . Aestivation: signaling and hypometabolism . J. Exp. Biol. , 215 ( 9 ): 1425 - 1433 , https://doi.org/10.1242/jeb.054403 https://doi.org/10.1242/jeb.054403 .

Sun D , Niu C J . 2012 . Adaptive significance of temperature-induced egg size plasticity in a planktonic rotifer, Brachionus calyciflorus . J. Plankton Res. , 34 ( 10 ): 864 - 873 , https://doi.org/10.1093/plankt/fbs050 https://doi.org/10.1093/plankt/fbs050 .

van der Weijden V A , Bulut-Karslioglu A . 2021 . Molecular regulation of paused pluripotency in early mammalian embryos and stem cells. Front Cell Dev . Biol ., 9 : 708318 , https://doi.org/10.3389/fcell.2021.708318 https://doi.org/10.3389/fcell.2021.708318 .

Vargas A L , Brazil T , Santangelo J M et al . 2024 . Long-term droughts change the hatching patterns of zooplankton resting eggs from permanent and temporary lakes . Freshwater Biol. , 69 ( 5 ): 635 - 644 , https://doi.org/10.1111/fwb.14234 https://doi.org/10.1111/fwb.14234 .

Xu H H , Niu C J . 2021 . Effect of maternal ammonia stress on population dynamics of the rotifer Brachionus calyciflorus offspring. Aquat . Toxicol ., 239 : 105960 , https://doi.org/10.1111/fwb.14234 https://doi.org/10.1111/fwb.14234 .

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

Changes in induced-antipredation defense traits and transcriptome regulation of rotifer Brachionus calyciflorus in response to nanoplastics

A preliminary study on life history of marine red alga Stylonema alsidii (Zandardini) Drew f. ramosum Zheng et Li

Responding of zooplankton to environmental factor changes in the Changjiang River estuarine regions in spring-summer from 2016 to 2020

The response of zooplankton abundance in saline meromictic Lake Shira to a change in circulation regime

高压涡轮封严流与主流相互作用的机理研究