Abstract
Global warming may pose a serious threat to seed germination and establishment in alpine ecosystems, given that temperature is a primary factor in stimulating seed germination and regulating changes in seed dormancy. However, to date, little is known about the relative importance of temperatures experienced by parents versus by the seeds (after dispersal). In this study, we tested the effects of warming at different stages on germination success and timing in the Australian alpine herb Wahlenbergia ceracea. To decouple the effect of parental warming from that of offspring warming, we raised parental plants (in both outcrossed and selfed lines) in both current (benign, cool) and future (warm) temperature conditions, and then sowed the seeds they produced back in either current or future conditions. We quantified (1) the effects of parental and/or offspring warming on (i) the percentage of germination and (ii) the season of germination (i.e. effects on dormancy); (2) whether the season of germination affected seedling growth; and (3) the effects of inbreeding and its interaction with temperature. We found that the percentage of germination decreased slightly with parental warming, but increased greatly with offspring warming. Parental warming also increased the fraction of dormant seeds, indicating a shift from predominately autumn to spring emergence. Spring-emerged seedlings grew slower than autumn-emerged seedlings, but the growth rate of spring-emerged seedlings were not detrimentally affected by warm offspring temperatures. In this facultatively autogamous species, inbreeding magnified the negative effects of both parental and offspring warming. Our results illustrate the value of tests of the effects of warming across generations and on multiple life stages for improving our understanding of the ecological processes behind plant germination and establishment, and of plant responses to climate warming.
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References
Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242. https://doi.org/10.1038/sj.hdy.6800721
Auge GA, Leverett LD, Edwards BR, Donohue K (2017) Adjusting phenotypes via within- and across-generational plasticity. New Phytol 216:343–349. https://doi.org/10.1111/nph.14495
Bates DM, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bernareggi G, Carbognani M, Mondoni A, Petraglia A (2016) Seed dormancy and germination changes of snowbed species under climate warming: the role of pre- and post-dispersal temperatures. Ann Bot 118:529–539. https://doi.org/10.1093/aob/mcw125
Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115. https://doi.org/10.1111/j.1461-0248.2007.01130.x
Briceño VF, Harris-Pascal D, Nicotra AB, Williams E, Ball MC (2014) Variation in snow cover drives differences in frost resistance in seedlings of the alpine herb Aciphylla glacialis. Environ Exp Bot 106:174–181. https://doi.org/10.1016/j.envexpbot.2014.02.011
Briceño VF, Hoyle GL, Nicotra AB (2015) Seeds at risk: How will a changing alpine climate affect regeneration from seeds in alpine areas? Alp Bot 125:59–68. https://doi.org/10.1007/s00035-015-0155-1
Carbognani M, Tomaselli M, Petraglia A (2018) Different temperature perception in high-elevation plants: new insight into phenological development and implications for climate change in the alpine tundra. Oikos 127:1014–1023. https://doi.org/10.1111/oik.04908
Cavieres LA, Sierra-Almeida A (2018) Assessing the importance of cold-stratification for seed germination in alpine plant species of the High-Andes of central Chile. Perspect Plant Ecol Evol Syst 30:125–131. https://doi.org/10.1016/j.ppees.2017.09.005
Chen M, MacGregor DR, Dave A, Florance H, Moore K, Paszkiewicz K, Smirnoff N, Graham IA, Penfield S (2014) Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year. Proc Natl Acad Sci USA 111:18787–18792. https://doi.org/10.1073/pnas.1412274111
Cheptou PO, Donohue K (2011) Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytol 189:395–407. https://doi.org/10.1111/j.1469-8137.2010.03541.x
Fernández-Pascual E, Jiménez-Alfaro B, Bueno Á (2017) Comparative seed germination traits in alpine and subalpine grasslands: higher elevations are associated with warmer germination temperatures. Plant Biol 19:32–40. https://doi.org/10.1111/plb.12472
Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258. https://doi.org/10.1111/j.1558-5646.2010.01108.x
Franke K, Fischer K (2013) Effects of inbreeding and temperature stress on life history and immune function in a butterfly. J Evol Biol 26:517–528. https://doi.org/10.1111/jeb.12064
Graae BJ, Alsos IG, Ejrnaes R (2008) The impact of temperature regimes on development, dormancy breaking and germination of dwarf shrub seeds from arctic, alpine and boreal sites. Plant Ecol 198:275–284. https://doi.org/10.1007/s11258-008-9403-4
Gremer JR, Venable DL (2014) Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment. Ecol Lett 17:380–387. https://doi.org/10.1111/ele.12241
Gremer JR, Chiono A, Suglia E, Bontrager M, Okafor L, Schmitt J (2020a) Variation in the seasonal germination niche across an elevational gradient: the role of germination cueing in current and future climates. Am J Bot 107:1–14. https://doi.org/10.1007/s11258-008-9403-4
Gremer JR, Wilcox CJ, Chiono A, Suglia E, Schmitt J (2020b) Germination timing and chilling exposure create contingency in life history and influence fitness in the native wildflower Streptanthus tortuosus. J Ecol 108:239–255. https://doi.org/10.1111/1365-2745.13241
Hegland SJ, Nielsen A, Lázaro A, Bjerknes A, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195. https://doi.org/10.1111/j.1461-0248.2008.01269.x
Hovenden MJ, Wills KE, Chaplin RE, Vander Schoor JK, Williams AL, Osanai Y, Newton PCD (2008) Warming and elevated CO2 affect the relationship between seed mass, germinability and seedling growth in Austrodanthonia caespitosa, a dominant Australian grass. Global Change Biol 14:1633–1641. https://doi.org/10.1111/j.1365-2486.2008.01597.x
Hoyle GL, Venn SE, Steadman KJ, Good RB, McAuliffe EJ, Williams ER, Nicotra AB (2013) Soil warming increases plant species richness but decreases germination from the alpine soil seed bank. Global Change Biol 19:1549–1561. https://doi.org/10.1111/gcb.12135
Hoyle GL, Steadman KJ, Good RB, McIntosh EJ, Galea LME, Nicotra AB (2015) Seed germination strategies: an evolutionary trajectory independent of vegetative functional traits. Front Plant Sci 6:731. https://doi.org/10.3389/fpls.2015.00731
Kendall S, Penfield S (2012) Maternal and zygotic temperature signalling in the control of seed dormancy and germination. Seed Sci Res 22:S23–S29. https://doi.org/10.1017/S0960258511000390
Klady RA, Henry GHR, Lemay V (2011) Changes in high arctic tundra plant reproduction in response to long-term experimental warming. Global Change Biol 17:1611–1624. https://doi.org/10.1111/j.1365-2486.2010.02319.x
Kochanek J, Steadman KJ, Probert RJ, Adkins SW (2011) Parental effects modulate seed longevity: exploring parental and offspring phenotypes to elucidate pre-zygotic environmental influences. New Phytol 191:223–233. https://doi.org/10.1111/j.1469-8137.2011.03681.x
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer
Lampei C, Metz J, Tielbörger K (2017) Clinal population divergence in an adaptive parental environmental effect that adjusts seed banking. New Phytol 2014:1230–1244. https://doi.org/10.1111/nph.14436
Leicht K, Jokela J, Seppälä O (2019) Inbreeding does not alter the response to an experimental heat wave in a freshwater snail. PLoS ONE 14:e0220669. https://doi.org/10.1371/journal.pone.0220669
Leimu R, Vergeer P, Angeloni F, Ouborg NJ (2010) Habitat fragmentation, climate change, and inbreeding in plants. Ann NY Acad Sci 1195:84–98. https://doi.org/10.1111/j.1749-6632.2010.05450.x
Milbau A, Graae BJ, Shevtsova A, Nijs I (2009) Effects of a warmer climate on seed germination in the subarctic. Ann Bot 104:287–296. https://doi.org/10.1093/aob/mcp117
Mondoni A, Rossi G, Orsenigo S, Probert RJ (2012) Climate warming could shift the timing of seed germination in alpine plants. Ann Bot 110:155–164. https://doi.org/10.1093/aob/mcs097
Mondoni A, Pedrini S, Bernareggi G, Rossi G, Abeli T, Probert RJ, Ghitti M, Bonomi C, Orsenigo S (2015) Climate warming could increase recruitment success in glacier foreland plants. Ann Bot 116:907–916. https://doi.org/10.1093/aob/mcv101
Nicotra AB, Segal DL, Hoyle GL, Schrey AW, Verhoeven KJF, Richards CL (2015) Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant. Ecol Evol 5:634–647. https://doi.org/10.1002/ece3.1329
Ohler LM, Lechleitner M, Junker RR (2020) Microclimatic effects on alpine plant communities and flower-visitor interactions. Sci Rep. https://doi.org/10.1038/s41598-020-58388-7 (article 1366)
Orsenigo S, Abeli T, Rossi G, Bonasoni P, Pasquaretta C, Gandini M, Mondoni A (2015) Effects of autumn and spring heat waves on seed germination of high mountain plants. PLoS ONE 10:e0133626. https://doi.org/10.1371/journal.pone.0133626
Penfield S (2017) Seed dormancy and germination. Curr Biol 27:PR874–PR878. https://doi.org/10.1016/S1369-5266(01)00219-9
Penfield S, MacGregor DR (2017) Effects of environmental variation during seed production on seed dormancy and germination. J Exp Bot 68:819–825. https://doi.org/10.1093/jxb/erw436
Satyanti A, Guja LK, Nicotra AB (2019) Temperature variability drives within-species variation in germination strategy and establishment characteristics of an alpine herb. Oecologia 189:407–419. https://doi.org/10.1007/s00442-018-04328-2
Schou MF, Bechsgaard J, Muñoz J, Kristensen TN (2018) Genome-wide regulatory deterioration impedes adaptive responses to stress in inbred populations of Drosophila melanogaster. Evolution 72:1614–1628. https://doi.org/10.1111/evo.13497
Schwienbacher E, Navarro-Cano JA, Neuner G, Erschbamer B (2011) Seed dormancy in alpine species. Flora 206:845–856. https://doi.org/10.1016/j.flora.2011.05.001
Springthorpe V, Penfield S (2015) Flowering time and seed dormancy control use external coincidence to generate life history strategy. eLife 4:e05557. https://doi.org/10.7554/eLife.05557
Starrfelt J, Kokko H (2012) Bet-hedging—a triple trade-off between means, variances and correlations. Biol Rev 87:742–755. https://doi.org/10.1111/j.1469-185X.2012.00225.x
Wadgymar SM, Mactavish RM, Anderson JT (2018) Transgenerational and within-generation plasticity in response to climate change: insights from a manipulative field experiment across an elevational gradient. Am Nat 192:698–714. https://doi.org/10.1086/700097
Wang GY, Baskin CC, Baskin JM, Yang XJ, Liu GF, Ye XH, Zhang XS, Huang ZY (2018) Effects of climate warming and prolonged snow cover on phenology of the early life history stages of four alpine herbs on the southeastern Tibetan Plateau. Am J Bot 105:967–976. https://doi.org/10.1002/ajb2.1104
Wheeler JA, Hoch G, Cortés AJ, Sedlacek J, Wipf S, Rixen C (2014) Increased spring freezing vulnerability for alpine shrubs under early snowmelt. Oecologia 175:219–229. https://doi.org/10.1007/s00442-013-2872-8
Xu J, Li WL, Zhang CH, Liu W, Du GZ (2017) The determinants of seed germination in an alpine/subalpine community on the Eastern Qinghai-Tibetan Plateau. Ecol Eng 98:114–122. https://doi.org/10.1016/j.ecoleng.2016.10.070
Acknowledgements
The authors thank all those who helped with lab work and discussions of the experiment, particularly Abigail Ryan, Annisa Satyanti, Joshua Hodges, Rocco Notarnicola, Zachary Brown, and the Plant Services staff of Research School of Biology at ANU. S.W. thanks the China Scholarship Council (CSC) for financial support. This study was supported by funding from the Australian Research Council (DP170101681).
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This study was supported by funding from the Australian Research Council (DP170101681).
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All the authors were involved in the background work and conception of the project. ABN, SW and KMG designed the experiment. SW and KMG performed the experiment and equally contributed to the data collection. SW performed data analyses and wrote the manuscript. LEBK, ABN and PAA contributed critically to the data analyses and interpretation. All the authors contributed to drafts.
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Wang, S., Gowland, K.M., Kruuk, L.E.B. et al. Decoupling the effects of parental and offspring warming on seed and seedling traits. Alp Botany 131, 105–115 (2021). https://doi.org/10.1007/s00035-021-00251-0
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DOI: https://doi.org/10.1007/s00035-021-00251-0