Abstract
A putative seed number/mass trade-off is fundamental to understanding the evolution of forest species and their capacity to recover from increasing losses to drought and harvest; however, such a trade-off is not always observed, and variation in this trade-off could arise if species face strong selection pressure for one or the other of these traits under different climatic factors. Yet to date few studies have considered the response of this trade-off to climatic gradients. In this study, three seed traits (seed mass, seed number, and seed abortion) at the cone level for 2,671 cones of Pinus yunnanensis collected from nine populations in the mountains of Southwest China were examined. The evidence for the potential trade-off between seed mass and number both within and across populations was assessed, In addition, the strength and direction of this trade-off along different climatic conditions was quantified. A significant negative relationship between seed mass and seed number was found across populations, which didn’t occur consistently within populations. Seed mass was strongly determined by seed abortion and the strength of the relationship between seed mass and seed abortion rate varied significantly among populations. Based on the climatic variables of populations, mean annual precipitation and temperature had a significant positive effect on seed mass and seed number, but a negative effect on seed abortion rate. However, the variation of filled seed number in the cone was much less than that of seed mass due to the stronger seed number/mass trade-off with decreasing mean annual precipitation. Thus, within populations, selection may be able to act more strongly on seed mass than on seed number in drier climate. We have found strong support for the intra-specific seed number/mass trade-off at the cone level of Pinus species. Importantly, the strength of this trade-off varied significantly among populations and seed abortion might affect seed mass through its association with this trade-off. Climatic factors generate selection both on seed mass and seed number, and the harsher climates (colder and drier climate) caused a reduction both in them. Our results highlight that climate conditions may co-vary or interact with life-history constraints, which potentially determines the natural population development and distribution.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
References
Adler PB, Salguero-Gómez R, Compagnoni A, Hsu JS, Ray-Mukherjee J, Mbeau-Ache C, Franco M (2014) Functional traits explain variation in plant life history strategies. Natl Acad Sci USA 111:740–745. https://doi.org/10.5061/dryad.8g252
Bramlett DL, Belcher EWJ, DeBarr GL, Hertel GD, Karrfalt RP, Lantz CW, Mller T, Ware KD, Yates HOI (1977) Cone analysis of southern pines: a guidebook. General Technical Report SE-13. Southeastern Forest Exp. Sta., Forest Service, USDA, Asheville, North Carolina
Brancalion PHS, Rodrigues RR (2014) Seed size-number trade-off in Euterpe edulis in plant communities of the Atlantic Forest. Sci Arg 71:226–231. https://doi.org/10.1590/S0103-90162014000300007
Cavers PB, Steel MG (1984) Patterns of change in seed weight over time on individual plants. Am Nat 124:324–335. https://doi.org/10.1086/284276
Chen F, Fan ZF, Niu SK, Zheng JM (2014) The influence of precipitation and consecutive dry days on burned areas in Yunnan Province, Southwestern China. Adv Meteorol 10:93–97. https://doi.org/10.1155/2014/748923
Cochrane A, Yates CJ, Hoyle GL, Nicotra AB (2015) Will among-population variation in seed traits improve the chance of species persistence under climate change? Global Ecol Biogeogr 24:12–24. https://doi.org/10.1111/geb.12234
Cochrane A, Hoyle GL, Yates CJ, Neeman T, Nictra AB (2016) Variation in plant functional traits across and within four species of Western Australian Banksia (Proteaceae) along a natural climate gradient. Austral Ecol 41:886–896. https://doi.org/10.1111/aec.12381
Cushman SA (2014) Grand challenges in evolutionary and population genetics: the importance of integrating epigenetics, genomics, modeling, and experimentation. Front Genet 5:197
Dani KGS, Kodandaramaiah U (2017) Plant and animal reproductive strategies: lessons from offspring size and number tradeoffs. Front Ecol Evol 5:38. https://doi.org/10.3389/fevo.2017.00038
Davis LE, Stephenson AG (1987) Pollen competition improves performance and reproductive output of the common zucchini squash under field conditions. J Am Soc Hort Sci 112:712–716. https://doi.org/10.21273/JASHS.112.4.712
Falster DS, Warton DI, Wright IJ (2006) User’s guide to SMATR: Standardised Major Axis Tests & Routines Version 2.0. http://www.bio.mq.edu.au/ecology/SMATR/
Fricke EC, Tewksbury JJ, Rogers HS (2019) Link intra-specific trait variation and plant function: seed size mediates performance tradeoffs within species. Oikos 128:1716–1725. https://doi.org/10.1111/oik.06494
Garcia D, Zamora R, Gómez JM, Jordano P, Hódar J (2000) Geographical variation in seed production, predation and abortion in Juniperus communis throughout its range in Europe. J Ecol 88:436–446. https://doi.org/10.1046/j.1365-2745.2000.00459.x
Garcia R, Siepielski AM, Benkman CW (2009) Cone and seed trait variation in whitebark pine (Pinus albicaulis; Pinaceae) and the potential for phenotypic selection. Am J Bot 96:1050–1054. https://doi.org/10.3732/ajb.0800298
Ghazoul J, Satake A (2009) Nonviable seed set enhances plant fitness: the sacrificial sibling hypothesis. Ecology 90:369–377. https://doi.org/10.1890/07-1436.1
Grotkopp E, Rejmánek M, Rost TL (2002) Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. Am Nat 159:396–419. https://doi.org/10.1086/338995
Guo H, Mazer S, Du G (2010) Geographic variation in seed mass within and among nine species of Pedicularis (Orobanchaceae): effects of elevation, plant size and seed number per fruit. J Ecol 98:1232–1242. https://doi.org/10.1111/j.1365-2745.2010.01688.x
Halpern SL (2005) Sources and consequences of seed size variation in Lupinus perennis (Fabaceae): adaptive and non-adaptive hypotheses. Am J Bot 92:205–213. https://doi.org/10.3732/ajb.92.2.205
Huang J, Chen B, Liu C, Lai J, Zhang J, Ma K (2012) Identifying hotspots of endemic woody seed plant diversity in China. Divers Distrib 18:673–688. https://doi.org/10.1111/j.1472-4642.2011.00845.x
Jin ZZ, Peng J (2004) Yunnan Pine. Yunnan Science and Technology Press, Kunming in Chinese
Kärkkäinen K, Savolainen O, Koski V (1999) Why do plants abort so many developing seeds: bad offspring or bad maternal genotypes? Evol Ecol 13:305–317. https://doi.org/10.1023/A:1006746900736
Koenig WD, Knops JMN, Carmen WJ, Sage RD (2009) No trade-off between seed size and number in the valley oak Quercus lobata. Am Nat 173:682–688. https://doi.org/10.1086/597605
Labouche AM, Richards SA, Pannell JR (2016) Effects of pollination intensity on offspring number and quality in a wind-pollinated herb. J Ecol 105:197–208. https://doi.org/10.1111/1365-2745.12659
Labra MH, Struik PC, Evers JB, Calderini DF (2017) Plasticity of seed weight compensates reductions in seed number of oilseed rape in response to shading at flowering. Eur J Agron 84:113–124. https://doi.org/10.1016/j.eja.2016.12.011
Lázaro A, Larrinaga AR (2018) A multi-level test of the seed number/size trade-off in two Scandinavian communities. PLoS ONE 13:e0201175. https://doi.org/10.1371/journal.pone.0201175
Lázaro A, Traveset A (2009) Does the spatial variation in selective pressures explain among-site differences in seed mass? A test with buxus balearica. Evol Ecol 23:847–865. https://doi.org/10.1007/s10682-008-9275-z
Leishman MR (2001) Does seed size/number trade-off model determine plant community structure? An assessment of the model mechanisms and their generality. Oikos 93:294–302. https://doi.org/10.1034/j.1600-0706.2001.930212.x
Leishman MR, Wright IJ, Moles AT, Westoby M (2000) The evolutionary ecology of seed size. In: Fenner M (ed) Seeds: the ecology of regelation in plant communities. CABI Publishing, Wallingford, pp 31–57
Liu Y, El-Kassaby YA (2020) Ecological drivers of plant life-history traits: assessment of seed mass and germination variation using climate cues and nitrogen resources in conifers. Ecol Indic 117:106517. https://doi.org/10.1016/j.ecolind.2020.106517
Liu J, Bai Y, Lamb EG, Simpson D, Liu G, Wei Y, Wang D, McKenney DW, Papadopol P (2013) Patterns of cross-continental variation in tree seed mass in the Canadian Boreal Forest. PLoS ONE 8:e61060. https://doi.org/10.1371/journal.pone.0061060
Liu Y, Wang T, El-Kassaby YA (2016) Contributions of dynamic environmental signals during life-cycle transitions to early life-history traits in lodgepole pine (Pinus contorta Dougl.). Biogeosciences 13:2945–2958. https://doi.org/10.5194/bg-13-2945-2016
Lloyd DG (1987) Selection of offspring size at independence and other size-versus-number strategies. Am Nat 129:800–817. https://doi.org/10.1086/284676
Mazer SJ, Park IM, Kimura M, Maul EM, Yim AM, Peach K (2020) Mating system and historical climate conditions affect population mean seed mass: evidence for adaptation and a new component of the selfing syndrome in Clarkia. J Ecol 108:1523–1539. https://doi.org/10.1111/1365-2745.13338
Melser C, Klinkhamer PGL (2001) Selective seed abortion increases offspring survival in Cynoglossum officinale (Boraginaceae). Am J Bot 88:1033–1040. https://doi.org/10.2307/2657085
Moles AT (2018) Being John Harper: using evolutionary ideas to improve understanding of global patterns in plant traits. J Ecol 106:1–18. https://doi.org/10.1111/1365-2745.12887
Murray BR, Brown AHD, Dickman CR, Crowther MS (2004) Geographical gradients in seed mass in relation to climate. J Biogeogr 31:379–388. https://doi.org/10.1046/j.0305-0270.2003.00993.x
Paul-Victor C, Turnbull LA (2009) The effect of growth conditions on the seed size/number trade-off. PLoS ONE 4:e6917. https://doi.org/10.1371/journal.pone.0006917
Roland CA, Schmidt JH, Johnstone JF (2014) Climate sensitivity of reproduction in a mast-seeding boreal conifer across its distributional range from lowland to treeline forests. Oecologia 174:665–677. https://doi.org/10.1007/s00442-013-2821-6
Saatkamp A, Cochrane A, Commander L, Guja LK, Jimenez-Alfaro B, Larson J, Nicotra A, Poschlod P, Silveira FAO, Cross AT, Dalziell EL, Dickie J, Erickson TE, Fidelis A, Fuchs A, Golos PJ, Hope M, Lewandrowski W, Merritt DJ, Miller BP, Miller RG, Offord CA, Ooi MKJ, Satyanti A, Sommerville KD, Tangney R, Tomlinson S, Turner S, Walck JL (2019) A research agenda for seed-trait functional ecology. New Phytol 221:1764–1775. https://doi.org/10.1111/nph.15502
Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506. https://doi.org/10.1086/282929
Sõber V, Ramula S (2013) Seed number and environmental conditions do not explain seed size variability for the invasive herb Lupinus polyphyllus. Plant Ecol 214:883–892. https://doi.org/10.1007/s11258-013-0216-8
Soper-Gorden NL, Winkler KJ, Jahnke MR, Marshall E, Horky J, Huddelson C, Etterson JR (2016) Geographic patterns of seed mass are associated with climate factors, but relationships vary between species. Am J Bot 103:60–72. https://doi.org/10.3732/ajb.1500295
Souza ML, Lovato MB, Fagundes M, Valladares F, Lemos-Filho JP (2019) Soil fertility and rainfall during specific phenological phases affect seed trait variation in a widely distributed Neotropical tree, Copaifera langsdorffii. Am J Bot 106:1096–1105. https://doi.org/10.1002/ajb2.1333
Tremayne MA, Richards AJ (2000) Seed weight and seed number affect subsequent fitness in outcrossing and selfing Primula species. New Phytol 148:127–142. https://doi.org/10.1046/j.1469-8137.2000.00738.x
Vaughton G, Ramsey M (1998) Sources and consequences of seed mass variation in Banksia marginata (Proteaceae). J Ecol 86:563–573. https://doi.org/10.1046/j.1365-2745.1998.00279.x
Venable DL (1992) Size-number trade-offs and the variation of seed size with plant resource status. Am Nat 140:287–304. https://doi.org/10.1086/285413
Wang B, Mao JF, Zhao W, Wang XR (2013) Impact of geography and climate on the genetic differentiation of the subtropical pine Pinus yunnanensis. PLoS ONE 8:e67345. https://doi.org/10.1371/journal.pone.0067345
Wang L, Meng L, Luo J (2015) Florivory modulates the seed number-seed weight relationship in Halenia elliptica (Gentianaceae). Sci World J 2015:610735. https://doi.org/10.1155/2015/610735
Wang T, Wang G, Innes JL, Seely B, Chen B (2017) ClimateAP: an application for dynamic local downscaling of historical and future climate data in Asia Pacific. Front Agric Sci Eng 4:448–458. https://doi.org/10.15302/J-FASE-2017172
Warton DI, Wright IJ, Falster DS, Westoby M (2010) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291. https://doi.org/10.1017/S1464793106007007
Wyse SV, Hulme PE (2021) Limited evidence for a consistent seed mass-dispersal trade-off in wind-dispersed pines. J Ecol 109:284–293. https://doi.org/10.1111/1365-2745.13477
Zheng J, Guo Z, Wang X (2017) Seed mass of angiosperm woody plants better explained by life history traits than climate across China. Sci Rep 7:2741. https://doi.org/10.1038/s41598-017-03076-2
Acknowledgements
The authors would like to thank Zhongyi Qin, Chaoben Yang, and Xuejia Lu for their invaluable assistance in the laboratory and the field investigation. This work was supported by the Essential Scientific Research of Chinese National Non-profit Institute (CAFYBB2019ZB006), National Natural Science Foundation of China (32001299), Yunnan Applied Basic Research Projects (2019FA013), and Training Objects of Technological Innovation Talents in Yunnan Province (2019HB074).
Funding
This work was supported by the Essential Scientific Research of Chinese National Non-profit Institute (CAFYBB2019ZB006), National Natural Science Foundation of China (32001299), Yunnan Applied Basic Research Projects (2019FA013), and Training Objects of Technological Innovation Talents in Yunnan Province (2019HB074).
Author information
Authors and Affiliations
Contributions
CG: writing—review and editing. FL: investigation. YM: validation. JL: methodology. ZL: software. KC: data curation.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Thomas Nagel.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gao, C., Liu, F., Miao, Y. et al. Variation in seed number/mass trade-off for Pinus yunnanensis along a natural climate gradient in the mountains of Southwest China. Plant Ecol 224, 203–219 (2023). https://doi.org/10.1007/s11258-023-01290-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-023-01290-9