Effects of Descendent Phenotypic Diversity Mediated by Ancestor Environmental Variation on Population Productivity of a Clonal Plant
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Species and Material Preparation
2.2. Experimental Design
2.3. Measurements
2.4. Data Analyses
3. Results
3.1. Growth Performance in Experiment 1
3.2. Growth Performance in Experiment 2
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Venail, P.; Gross, K.; Oakley, T.H.; Narwani, A.; Allan, E.; Flombaum, P.; Isbell, F.; Joshi, J.; Reich, P.B.; Tilman, D.; et al. Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct. Ecol. 2015, 29, 615–626. [Google Scholar] [CrossRef]
- Isbell, F.; Cowles, J.; Dee, L.E.; Loreau, M.; Reich, P.B.; Gonzalez, A.; Hector, A.; Schmid, B. Quantifying effects of biodiversity on ecosystem functioning across times and places. Ecol. Lett. 2018, 21, 763–778. [Google Scholar] [CrossRef] [PubMed]
- Loreau, M.; Hector, A. Partitioning selection and complementarity in biodiversity experiments. Nature 2001, 412, 72–76. [Google Scholar] [CrossRef] [PubMed]
- Loreau, M.; Naeem, S.; Inchausti, P. Biodiversity and ecosystem functioning: Synthesis and perspectives. Restor. Ecol. 2002, 12, 611–612. [Google Scholar]
- Ratcliffe, S.; Wirth, C.; Jucker, T.; Plas, F.V.D.; Scherer-Lorenzen, M.; Verheyen, K.; Allan, E.; Benavides, R.; Bruelheide, H.; Ohse, B.; et al. Biodiversity and ecosystem functioning relations in European forests depend on environmental context. Ecol. Lett. 2017, 20, 1414–1426. [Google Scholar] [CrossRef]
- Hughes, A.R.; Inouye, B.D.; Johnson, M.T.J.; Underwood, N.; Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 2008, 11, 609–623. [Google Scholar] [CrossRef]
- Chalmandrier, L.; Albouy, C.; Pellissier, L. Species pool distributions along functional trade-offs shape plant productivity–diversity relationships. Sci. Rep. 2017, 7, 15405. [Google Scholar] [CrossRef]
- Engbersen, N.; Stefan, L.; Brooker, R.W.; Schöb, C. Using plant traits to understand the contribution of biodiversity effects to annual crop community productivity. Ecol. Appl. 2022, 32, e02479. [Google Scholar] [CrossRef]
- Allan, E.; Weisser, W.; Weigelt, A.; Roscher, C.; Fischer, M.; Hillebrand, H. More diverse plant communities have higher functioning over time due to turnover in complementary dominant species. Proc. Natl. Acad. Sci. USA 2011, 108, 17034–17039. [Google Scholar] [CrossRef]
- Wang, X.; Wang, J.; Hu, B.; Zheng, W.L.; Li, M.; Shen, Z.X.; Yu, F.H.; Schmid, B.; Li, M.H. Richness, not evenness, of invasive plant species promotes invasion success into native plant communities via selection effects. Oikos 2022, 2022, e08966. [Google Scholar] [CrossRef]
- Fargione, J.; Tilman, D.; Dybzinski, R.; Lambers, J.H.R.; Clark, C.; Harpole, W.S.; Knops, J.M.H.; Reich, P.B.; Loreau, M. From selection to complementarity: Shifts in the causes of biodiversity–productivity relationships in a long-Term biodiversity experiment. Proc. R. Soc. B 2007, 274, 871–876. [Google Scholar] [CrossRef] [PubMed]
- Eisenhauer, N. Aboveground–belowground interactions as a source of complementarity effects in biodiversity experiments. Plant Soil 2011, 351, 1–22. [Google Scholar] [CrossRef]
- Bakker, L.M.; Mommer, L.; Ruijven, J.V. Can root trait diversity explain complementarity effects in a grassland biodiversity experiment? J. Plant Ecol. 2018, 11, 73–84. [Google Scholar] [CrossRef]
- Tilman, D.; Reich, P.B.; Knops, J.; Wedin, D.; Mielke, T.; Lehman, C. Diversity and productivity in a long-term grassland experiment. Science 2001, 294, 843–845. [Google Scholar] [CrossRef] [PubMed]
- Schöb, C.; Kerle, S.; Karley, A.J.; Morcillo, L.; Pakeman, R.J.; Newton, A.C.; Brooker, R.W. Intraspecific genetic diversity and composition modify species-level diversity-productivity relationships. New Phytol. 2015, 205, 720–730. [Google Scholar] [CrossRef] [PubMed]
- Vermeulen, P.J.; Anten, N.P.R.; Schieving, F.; Werger, M.J.A.; During, H.J. Height convergence in response to neighbour growth: Genotypic differences in the stoloniferous plant Potentilla reptans. New Phytol. 2008, 177, 688–697. [Google Scholar] [CrossRef]
- Cadotte, M.W. Functional traits explain ecosystem function through opposing mechanisms. Ecol. Lett. 2017, 20, 989–996. [Google Scholar] [CrossRef]
- Badyaev, A.V.; Uller, T. Parental effects in ecology and evolution: Mechanisms, processes and implications. Phil. Trans. R. Soc. B 2009, 364, 1169–1177. [Google Scholar] [CrossRef] [PubMed]
- Portela, R.; Dong, B.-C.; Yu, F.-H.; Barreiro, R.; Roiloa, S.R.; Matos, D.M.S. Trans-generational effects in the clonal invader Alternanthera philoxeroides. J. Plant Ecol. 2020, 13, 122–129. [Google Scholar] [CrossRef]
- DuBois, K.; Williams, S.L.; Stachowicz, J.J. Previous exposure mediates the response of eelgrass to future warming via clonal transgenerational plasticity. Ecology 2020, 101, e03169. [Google Scholar] [CrossRef]
- Dong, B.-C.; Kleunen, M.V.; Yu, F.-H. Context-dependent parental effects on clonal offspring performance. Front. Plant Sci. 2018, 9, 1824. [Google Scholar] [CrossRef] [PubMed]
- Dong, B.-C.; Yu, F.-H.; Roiloa, S.R. Editorial: Ecoepigenetics in clonal and inbreeding plants: Transgenerational adaptation and environmental variation. Front. Plant Sci. 2019, 10, 622. [Google Scholar] [CrossRef] [PubMed]
- Dong, B.-C.; Wang, M.-Z.; Liu, R.-H.; Luo, F.-L.; Li, H.-L.; Yu, F.-H. Direct and legacy effects of herbivory on growth and physiology of a clonal plant. Biol. Invasions 2018, 20, 3631–3645. [Google Scholar] [CrossRef]
- Yadav, N.S.; Titov, V.; Ayemere, I.; Byeon, B.; Ilnytskyy, Y.; Kovalchuk, I. Multigenerational exposure to heat stress induces phenotypic resilience, and genetic and epigenetic variations in Arabidopsis thaliana offspring. Front. Plant Sci. 2022, 13, 728167. [Google Scholar] [CrossRef]
- Yu, W.-H.; Zhang, L.-M.; Luo, F.-L.; Yu, F.-H.; Li, M. Roles of clonal parental effects in regulating interspecific competition between two floating plants. Front. Plant Sci. 2022, 13, 924001. [Google Scholar] [CrossRef]
- Dong, B.-C.; Meng, J.; Yu, F.-H. Effects of parental light environment on growth and morphological responses of clonal offspring. Plant Biol. 2019, 21, 1083–1089. [Google Scholar] [CrossRef]
- Dong, B.-C.; Alpert, P.; Yu, F.-H. Transgenerational effects of herbivory and soil nutrients transmitted via vegetative reproduction in the clonal plant Alternanthera philoxeroides. Perspect. Plant Ecol. 2019, 41, 125498. [Google Scholar] [CrossRef]
- Dechaine, J.M.; Brock, M.T.; Weinig, C. Maternal environmental effects of competition influence evolutionary potential in rapeseed (Brassica rapa). Evol. Ecol. 2015, 29, 77–91. [Google Scholar] [CrossRef]
- Li, C.; Wang, T.; Zhang, M.; Xu, J. Maternal environment effect of warming and eutrophication on the emergence of curled pondweed, Potamogeton crispus L. Water 2018, 10, 1285. [Google Scholar] [CrossRef]
- Latzel, V.; Klimešová, J. Transgenerational plasticity in clonal plants. Evol. Ecol. 2010, 24, 1537–1543. [Google Scholar] [CrossRef]
- Zhang, L.-M.; Roiloa, S.R.; Zhang, J.-F.; Yu, W.-H.; Qiu, C.-Y.; Wang, D.-H.; Yu, F.-H. Clonal parental effects on offspring growth of different vegetative generations in the aquatic plant Pistia stratiotes. Front. Plant Sci. 2022, 13, 890309. [Google Scholar] [CrossRef]
- Kuijper, B.; Johnstone, R.A. Maternal effects and parent-offspring conflict. Evolution 2018, 72, 220–233. [Google Scholar] [CrossRef] [PubMed]
- Latzel, V.; Janeček, Š.; Doležal, J.; Klimešová, J.; Bossdorf, O. Adaptive transgenerational plasticity in the perennial Plantago lanceolata. Oikos 2014, 123, 41–46. [Google Scholar] [CrossRef]
- Fort, T.; Pauvert, C.; Zanne, A.E.; Ovaskainen, O.; Caignard, T.; Barret, M.; Compant, S.; Hampe, A.; Delzon, S.; Vacher, C. Maternal effects shape the seed mycobiome in Quercus petraea. New Phytol. 2020, 230, 1594–1608. [Google Scholar] [CrossRef] [PubMed]
- Dong, B.-C.; Fu, T.; Luo, F.-L.; Yu, F.-H. Herbivory-iInduced maternal effects on growth and defense traits in the clonal species Alternanthera philoxeroides. Sci. Total Environ. 2017, 605, 114–123. [Google Scholar] [CrossRef] [PubMed]
- Zhou, X.H.; Li, J.J.; Gao, Y.Y.; Peng, P.H.; He, W.M. Maternal effects of climate warming and nitrogen deposition vary with home and introduced ranges. Funct. Ecol. 2021, 36, 751–762. [Google Scholar] [CrossRef]
- Jiang, L.; Wen, Z.; Zhang, Y.; Zhao, Z.; Tanveer, M.; Tian, C.; Wang, L. Transgenerational effects of maternal water condition on the growth, C:N stoichiometry and seed characteristics of the desert annual Atriplex aucheri. Plants 2021, 10, 2362. [Google Scholar] [CrossRef]
- Jacobs, D.L. An ecological life-history of Spirodela Polyrhiza (greater duckweed) with emphasis on the turion phase. Ecol. Monogr. 1947, 17, 437–469. [Google Scholar] [CrossRef]
- Magone, I. The effect of electromagnetic radiation from the Skrunda Radio Location Station on Spirodela polyrhiza (L.) Schleiden cultures. Sci. Total Environ. 1996, 180, 75–80. [Google Scholar] [CrossRef]
- Landolt, E. The Family of Lemnaceae—A Monographic Study; Veroeffentlichugen des Geobotanisches Institutes ETH: Zurich, Switzerland, 1986; Volume 1. [Google Scholar]
- Hillman, W.S. The Lemnaceae, or duckweeds: A review of the descriptive and experimental literature. Bot. Rev. 1961, 27, 221–287. [Google Scholar] [CrossRef]
- Vermaat, J.E.; Hanif, M.K. Performance of common duckweed species (Lemnaceae) and the waterfern Azolla filiculoides on different types of waste water. Water Res. 1998, 32, 2569–2576. [Google Scholar] [CrossRef]
- Lemon, G.D.; Posluszny, U.; Husband, B.C. Potential and realized rates of vegetative reproduction in Spirodela polyrhiza, Lemna minor, and Wolffia borealis. Aquat. Bot. 2001, 70, 79–87. [Google Scholar] [CrossRef]
- Wang, W.; Haberer, G.; Gundlach, H.; GläΒer, C.; Nussbaumer, T.; Luo, M.C.; Lomsadze, A.; Borodovsky, M.; Kerstetter, R.A.; Shanklin, J.; et al. The Spirodela polyrhiza genome reveals insights into its neotenous reduction fast growth and aquatic lifestyle. Nat. Commun. 2014, 5, 3311. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.-M.; Jin, Y.; Yao, S.-M.; Lei, N.-F.; Chen, J.-S.; Zhang, Q.; Yu, F.-H. Growth and morphological responses of duckweed to clonal fragmentation, nutrient availability and population density. Front. Plant Sci. 2020, 11, 618. [Google Scholar] [CrossRef]
- Lemon, G.D.; Posluszny, U. Comparative shoot development and evolution in the Lemnaceae. Int. J. Plant Sci. 2000, 161, 733–748. [Google Scholar] [CrossRef]
- Xing, W.; Huang, W.M.; Liu, G.H. Effect of excess iron and copper on physiology of aquatic plant Spirodela polyrrhiza (L.) Schleid. Environ. Toxicol. 2010, 25, 103–112. [Google Scholar]
- Hoagland, D.R.; Arnon, D.I. The water-culture method for growing plants without soil. Calif. Agric. Exp. Stn. Circ. 1950, 347, 1–32. [Google Scholar]
- Jin, Y.; Zhang, Q.; Zhang, L.-M.; Lei, N.-F.; Chen, J.-S.; Xue, W.; Yu, F.-H. Distinct responses of frond and root to increasing nutrient availability in a floating clonal plant. PLoS ONE 2021, 16, e0258253. [Google Scholar] [CrossRef]
- Zhu, Z.J.; Yuan, H.Z.; Wei, Y.; Li, P.S.; Zhang, P.H.; Xie, D. Effects of ammonia nitrogen and sediment nutrient on growth of the submerged plant Vallisneria natans. Clean Soil Air Water 2015, 43, 1653–1659. [Google Scholar] [CrossRef]
- Si, C.; Xue, W.; Lin, J.; Zhang, J.-F.; Yu, F.-H. No evidence of greater biomass allocation to stolons at moderate resource levels in a floating plant. Aquat. Ecol. 2020, 54, 421–429. [Google Scholar] [CrossRef]
- Krouk, G.; Ruffel, S.; Gutiérrez, R.A.; Gojon, A.; Crawford, N.M.; Coruzzi, G.M.; Lacombe, B. A framework integrating plant growth with hormones and nutrients. Trends Plant Sci. 2011, 16, 178–182. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.-M.; Yao, S.-M.; Jin, Y.; Song, M.-H.; Lei, N.-F.; Chen, J.-S.; Yu, F.-H. Effects of clonal fragmentation and nutrient availability on the competitive ability of the floating plant Salvinia natans. Folia Geobot. 2020, 55, 63–71. [Google Scholar] [CrossRef]
- Tan, B.-C.; He, H.; Gu, J.; Li, K.-Y. Effects of nutrient levels and light intensity on aquatic macrophyte (Myriophyllum aquaticum) grown in floating-Bed platform. Ecol. Eng. 2019, 128, 27–32. [Google Scholar] [CrossRef]
- Si, C.; Zhang, L.-M.; Yu, F.-H. Effects of physical space and nutrients on the growth and intraspecific competition of a floating fern. Aquat. Ecol. 2019, 53, 295–302. [Google Scholar] [CrossRef]
- Podgórska, A.; Burian, M.; Gieczewska, K.; Ostaszewska-Bugajska, M.; Zebrowski, J.; Solecka, D.; Szal, B. Altered cell wall plasticity can restrict plant growth under ammonium nutrition. Front. Plant Sci. 2017, 8, 1344. [Google Scholar] [CrossRef]
- Westerband, A.C.; Funk, J.L.; Barton, K.E. Intraspecific trait variation in plants: A renewed focus on its role in ecological processes. Ann. Bot. 2021, 127, 397–410. [Google Scholar] [CrossRef]
- Laughlin, D.C.; Gremer, J.R.; Adler, P.B.; Mitchell, R.M.; Moore, M.M. The net effect of functional traits on fitness. Trends Ecol. Evol. 2020, 35, 1037–1047. [Google Scholar] [CrossRef] [PubMed]
- Callaghan, T.V.; Carlsson, B.Å.; Jónsdóttir, I.S.; Svensson, B.M.; Jonasson, S. Clonal plants and environmental change: Introduction to the proceedings and summary. Oikos 1992, 63, 341–347. [Google Scholar] [CrossRef]
- Franklin, S.; Alpert, P.; Salguero-Gómez, R.; Janovský, Z.; Herben, T.; Klimešová, J.; Douhovnikoff, V. Next-gen plant clonal ecology. Perspect. Plant Ecol. 2021, 49, 125601. [Google Scholar] [CrossRef]
- Appenroth, K.J.; Ziegler, P. Light-induced degradation of storage starch in turions of Spirodela polyrhiza depends on nitrate. Plant Cell Environ. 2008, 31, 1460–1469. [Google Scholar] [CrossRef]
- Arnaud, M.; Jean-Philippe, B.; José, E.; Grégory, M. Rapid plant invasion in distinct climates involves different sources of phenotypic variation. PLoS ONE 2013, 8, e55627. [Google Scholar]
- Roach, D.A.; Wulff, R.D. Maternal effects in plants. Annu. Rev. Ecol. Syst. 1987, 18, 209–235. [Google Scholar] [CrossRef]
- Dodd, R.S.; Douhovnikoff, V. Adjusting to global change through clonal growth and epigenetic variation. Front. Ecol. Evol. 2016, 4, 86. [Google Scholar] [CrossRef]
- Baker, B.H.; Berg, L.J.; Sultan, S.E. Context-dependent developmental effects of parental shade versus sun are mediated by DNA methylation. Front. Plant Sci. 2018, 9, 1251. [Google Scholar] [CrossRef] [PubMed]
Effect | df | Total Mass | No. of Ramets |
---|---|---|---|
Nutrient availability (N) | 1, 77 | 544.8 *** | 422.3 *** |
Phenotypic diversity (D) | 3, 11 | 0.2 ns | 0.4 ns |
N × D | 3, 77 | 0.5 ns | 1.0 ns |
Effect | df | Total Mass | No. of Ramets | Mass per Ramet |
---|---|---|---|---|
Nutrient availability (N) | 3, 176 | 394.5 *** | 94.1 *** | 108.8 *** |
Initial density (D) | 1, 176 | 1035.8 *** | 1670.1 *** | 8.9 ** |
Light intensity (L) | 1, 176 | 3588.9 *** | 3300.8 *** | 1.5 ns |
N × D | 3, 176 | 9.5 *** | 5.3 ** | 0.7 ns |
N × L | 3, 176 | 212.3 *** | 20.0 *** | 33.0 *** |
D × L | 1, 176 | 98.4 *** | 284.6 *** | 1.5 ns |
N × D × L | 3, 176 | 2.5 ns | 8.5 *** | 3.3 * |
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Jin, Y.; Chen, J.-S.; Luo, F.-L.; Huang, L.; Lei, N.-F.; Yu, F.-H. Effects of Descendent Phenotypic Diversity Mediated by Ancestor Environmental Variation on Population Productivity of a Clonal Plant. Diversity 2022, 14, 616. https://doi.org/10.3390/d14080616
Jin Y, Chen J-S, Luo F-L, Huang L, Lei N-F, Yu F-H. Effects of Descendent Phenotypic Diversity Mediated by Ancestor Environmental Variation on Population Productivity of a Clonal Plant. Diversity. 2022; 14(8):616. https://doi.org/10.3390/d14080616
Chicago/Turabian StyleJin, Yu, Jin-Song Chen, Fang-Li Luo, Lin Huang, Ning-Fei Lei, and Fei-Hai Yu. 2022. "Effects of Descendent Phenotypic Diversity Mediated by Ancestor Environmental Variation on Population Productivity of a Clonal Plant" Diversity 14, no. 8: 616. https://doi.org/10.3390/d14080616