Variation in the seasonal germination niche across an elevational gradient: the role of germination cueing in current and future climates.
Arabidopsis
Streptanthus tortuosus
Brassicaceae
climate change
dormancy
germination temperature
niche construction
phenology
plasticity
stratification
Journal
American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
16
05
2019
accepted:
07
10
2019
pubmed:
15
2
2020
medline:
17
4
2020
entrez:
15
2
2020
Statut:
ppublish
Résumé
The timing of germination has profound impacts on fitness, population dynamics, and species ranges. Many plants have evolved responses to seasonal environmental cues to time germination with favorable conditions; these responses interact with temporal variation in local climate to drive the seasonal climate niche and may reflect local adaptation. Here, we examined germination responses to temperature cues in Streptanthus tortuosus populations across an elevational gradient. Using common garden experiments, we evaluated differences among populations in response to cold stratification (chilling) and germination temperature and related them to observed germination phenology in the field. We then explored how these responses relate to past climate at each site and the implications of those patterns under future climate change. Populations from high elevations had stronger stratification requirements for germination and narrower temperature ranges for germination without stratification. Differences in germination responses corresponded with elevation and variability in seasonal temperature and precipitation across populations. Further, they corresponded with germination phenology in the field; low-elevation populations germinated in the fall without chilling, whereas high-elevation populations germinated after winter chilling and snowmelt in spring and summer. Climate-change forecasts indicate increasing temperatures and decreasing snowpack, which will likely alter germination cues and timing, particularly for high-elevation populations. The seasonal germination niche for S. tortuosus is highly influenced by temperature and varies across the elevational gradient. Climate change will likely affect germination timing, which may cascade to influence trait expression, fitness, and population persistence.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
350-363Subventions
Organisme : UC Davis
Pays : International
Organisme : USDA
Pays : International
Organisme : NSF
ID : 1831913
Pays : International
Informations de copyright
© 2020 Botanical Society of America.
Références
Aitken, S. N., S. Yeaman, J. A. Holliday, T. Wang, and S. Curtis-McLane. 2008. Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary Applications 1: 95-111.
Angert, A. L., T. E. Huxman, P. Chesson, and D. L. Venable. 2009. Functional tradeoffs determine species coexistence via the storage effect. Proceedings of the National Academy of Sciences, USA 106: 11641-11645.
Antonovics, J., and P. H. Vantienderen. 1991. Ontoecogenophyloconstraints? The chaos of constraint terminology. Trends in Ecology & Evolution 6: 166-168.
Arene, F., L. Affre, A. Doxa, and A. Saatkamp. 2017. Temperature but not moisture response of germination shows phylogenetic constraints while both interact with seed mass and lifespan. Seed Science Research 27: 110-120.
Auge, G. A., L. D. Leverett, B. R. Edwards, and K. Donohue. 2017. Adjusting phenotypes via within- and across-generational plasticity. New Phytologist 216: 343-349.
Baldwin, B. G. 2014. Origins of plant diversity in the California Floristic Province. Annual Review of Ecology, Evolution, and Systematics 45: 347-369.
Barga, S., T. E. Dilts, and E. A. Leger. 2017. Climate variability affects the germination strategies exhibited by arid land plants. Oecologia 185: 437-452.
Baskin, C., and J. Baskin. 2014. Seeds: Ecology, biogeography and evolution of dormancy and germination. Academic Press, San Diego, CA, USA.
Bates, D., M. Maechler, B. Boker, and S. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1-48.
Bonamour, S., L.-M. Chevin, A. Charmantier, and C. Teplitsky. 2019. Phenotypic plasticity in response to climate change: the importance of cue variation. Philosophical Transactions of the Royal Society, B, Biological Sciences 374: 20180178.
Botero, C. A., F. J. Weissing, J. Wright, and D. R. Rubenstein. 2015. Evolutionary tipping points in the capacity to adapt to environmental change. Proceedings of the National Academy of Sciences, USA 112: 184-189.
Burghardt, L. T., C. J. E. Metcalf, A. M. Wilczek, J. Schmitt, and K. Donohue. 2015. Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes. American Naturalist 185: 212-227.
Calflora. 2014. Calflora: Information on California plants for education, research and conservation. The Calflora Database [a non-profit organization], Berkeley, CA, USA.
Cavieres, L. A., and M. T. K. Arroyo. 2000. Seed germination response to cold stratification period and thermal regime in Phacelia secunda (Hydrophyllaceae) - altitudinal variation in the mediterranean Andes of central Chile. Plant Ecology 149: 1-8.
Cavieres, L. A., and A. Sierra-Almeida. 2018. Assessing the importance of cold-stratification for seed germination in alpine plant species of the High-Andes of central Chile. Perspectives in Plant Ecology, Evolution and Systematics 30: 125-131.
Cayan, D. R., E. P. Maurer, M. D. Dettinger, M. Tyree, and K. Hayhoe. 2008. Climate change scenarios for the California region. Climatic Change 87: 21-42.
Cochrane, A., C. J. Yates, G. L. Hoyle, and A. B. Nicotra. 2015. Will among-population variation in seed traits improve the chance of species persistence under climate change? Global Ecology and Biogeography 24: 12-24.
Cohen, D. 1966. Optimizing reproduction in a randomly varying environment. Journal of Theoretical Biology 12: 119-129.
Cohen, D. 1967. Optimizing reproduction in a randomly varying environment when a correlation may exist between the conditions at the time a choice has to be made and the subsequent outcome. Journal of Theoretical Biology 16: 1-14.
Cuello, W. S., J. R. Gremer, P. C. Trimmer, A. Sih, and S. J. Schreiber. 2019. Predicting evolutionarily stable strategies from functional responses of Sonoran Desert annuals to precipitation. Proceedings of the Royal Society, B, Biological Sciences 286: 20182613.
Dalgleish, H. J., D. N. Koons, and P. B. Adler. 2010. Can life-history traits predict the response of forb populations to changes in climate variability? Journal of Ecology 98: 209-217.
Debieu, M., C. Tang, B. Stich, T. Sikosek, S. Effgen, E. Josephs, J. Schmitt, et al. 2013. Co-variation between seed dormancy, growth rate and flowering time changes with latitude in Arabidopsis thaliana. PLOS One 8: e61075.
Donaldson-Matasci, M. C., C. T. Bergstrom, and M. Lachmann. 2013. When unreliable cues are good enough. American Naturalist 182: 313-327.
Donohue, K. 2002. Germination timing influences natural selection on life-history characters in Arabidopsis thaliana. Ecology 83: 1006-1016.
Donohue, K., D. Dorn, C. Griffith, E. Kim, A. Aguilera, C. R. Polisetty, and J. Schmitt. 2005a. Niche construction through germination cueing: life-history responses to timing of germination in Arabidopsis thaliana. Evolution 59: 771-785.
Donohue, K., L. Dorn, C. Griffith, E. Kim, A. Aguilera, C. R. Polisetty, and J. Schmitt. 2005b. The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution 59: 758-770.
Donohue, K., R. R. de Casas, L. Burghardt, K. Kovach, and C. G. Willis. 2010. Germination, postgermination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution, and Systematics 41: 293-319.
Eckhart, V. M., M. A. Geber, W. F. Morris, E. S. Fabio, P. Tiffin, and D. A. Moeller. 2011. The geography of demography: Long-term demographic studies and species distribution models reveal a species border limited by adaptation. American Naturalist 178: S26-S43.
Fenner, M., and K. Thompson. 2005. The ecology of seeds. Cambridge University Press, Cambridge, UK.
Fernández-Pascual, E., A. Pérez-Arcoiza, J. A. Prieto, and T. E. Díaz. 2017. Environmental filtering drives the shape and breadth of the seed germination niche in coastal plant communities. Annals of Botany 119: 1169-1177.
Finch-Savage, W. E., and S. Footitt. 2017. Seed dormancy cycling and the regulation of dormancy mechanisms to time germination in variable field environments. Journal of Experimental Botany 68: 843-856.
Finch-Savage, W. E., and G. Leubner-Metzger. 2006. Seed dormancy and the control of germination. New Phytologist 171: 501-523.
Flint, L. E., and A. L. Flint. 2014. California Basin characterization model: a dataset of historical and future hydrologic response to climate change., data release version 1.1. U.S. Geological Survey, Washington, D.C., USA. Available at https://ca.water.usgs.gov/projects/reg_hydro/basin-characterization-model.html.
Footitt, S., Z. Huang, H. A. Clay, A. Mead, and W. E. Finch-Savage. 2013. Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling, resulting in winter and summer annual phenotypes. The Plant Journal 74: 1003-1015.
Footitt, S., Z. Huang, H. Ölcer-Footitt, H. Clay, and W. E. Finch-Savage. 2018. The impact of global warming on germination and seedling emergence in Alliaria petiolata, a woodland species with dormancy loss dependent on low temperature. Plant Biology 20: 682-690.
Galloway, L. F., and K. S. Burgess. 2009. Manipulation of flowering time: phenological integration and maternal effects. Ecology 90: 2139-2148.
Galloway, L. F., and J. R. Etterson. 2007. Transgenerational plasticity is adaptive in the wild. Science 318: 1134-1136.
Gremer, J. R., and D. L. Venable. 2014. Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment. Ecology Letters 17: 380-387.
Gremer, J. R., S. Kimball, and D. L. Venable. 2016. Within- and among-year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment. Ecology Letters 19: 1209-1218.
Gremer, J. R., C. J. Wilcox, A. Chiono, E. Suglia, and J. Schmitt. 2020. Germination timing and chilling exposure create contingency in life history and influence fitness in the native wildflower Streptanthus tortuosus. Journal of Ecology 108: 239-255.
Hereford, J., J. Schmitt, and D. D. Ackerly. 2017. The seasonal climate niche predicts phenology and distribution of an ephemeral annual plant, Mollugo verticillata. Journal of Ecology 105: 1323-1334.
Hernández, F., M. Poverene, A. Garayalde, and A. Presotto. 2019. Re-establishment of latitudinal clines and local adaptation within the invaded area suggest rapid evolution of seed traits in Argentinean sunflower (Helianthus annuus L.). Biological Invasions 21: 2599-2612.
Huang, Z., S. Liu, K. J. Bradford, T. E. Huxman, and D. L. Venable. 2016. The contribution of germination functional traits to population dynamics of a desert plant community. Ecology 97: 250-261.
IPCC [Intergovernmental Panel on Climate Change]. 2014. Climate Change 2014: Impacts, adaptation, and vulnerability. Part B: Regional aspects. In V. R. Barros, C. B. Field, D. J. Dokken, M. D. Mastrandrea, K. J. Mach, T. E. Bilir, et al. [eds.], Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.
Kalisz, S. 1986. Variable selection on the timing of germination in Collinsia verna (Scrophulariaceae). Evolution 40: 479-491.
Kalisz, S., and M. A. McPeek. 1992. Demography of an age-structured annual- Resampled projection matrices, elasticity analyses, and seed bank effects. Ecology 73: 1082-1093.
Kimball, S., A. L. Angert, T. E. Huxman, and D. L. Venable. 2010. Contemporary climate change in the Sonoran Desert favors cold-adapted species. Global Change Biology 16: 1555-1565.
Kimball, S., A. L. Angert, T. E. Huxman, and D. L. Venable. 2011. Differences in the timing of germination and reproduction relate to growth physiology and population dynamics of Sonoran Desert winter annuals. American Journal of Botany 98: 1773-1781.
Kopp, M., and S. Matuszewski. 2014. Rapid evolution of quantitative traits: theoretical perspectives. Evolutionary Applications 7: 169-191.
Korves, T. M., K. Schmidt, A. L. Caicedo, C. Mays, J. R. Stinchcombe, M. D. Purugganan, and J. Schmitt. 2007. Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. American Naturalist 169: E141-E157.
Lampei, C., and K. Tielborger. 2010. Evolvability of between-year seed dormancy in populations along an aridity gradient. Biological Journal of the Linnean Society 100: 924-934.
Lampei, C., J. Metz, and K. Tielbörger. 2017. Clinal population divergence in an adaptive parental environmental effect that adjusts seed banking. New Phytologist 214: 1230-1244.
Levine, J. M., A. K. McEachern, and C. Cowan. 2011. Seasonal timing of first rain storms affects rare plant population dynamics. Ecology 92: 2236.
Loarie, S. R., B. E. Carter, K. Hayhoe, S. McMahon, R. Moe, C. A. Knight, and D. D. Ackerly. 2008. Climate change and the future of California's endemic flora. Plos One 3: e2502.
López, A. S., P. Marchelli, D. Batlla, D. R. López, and M. V. Arana. 2019. Seed responses to temperature indicate different germination strategies among Festuca pallescens populations from semi-arid environments in North Patagonia. Agricultural and Forest Meteorology 272-273: 81-90.
Luedeling, E. 2019. chillR: Statistical methods for phenology analysis in temperate fruit trees, version 0.70.15.
Maher, S. P., T. L. Morelli, M. Hershey, A. L. Flint, L. E. Flint, C. Moritz, and S. R. Beissinger. 2017. Erosion of refugia in the Sierra Nevada meadows network with climate change. Ecosphere 8: e01673.
Mayfield, M. M., J. M. Dwyer, A. Main, and J. M. Levine. 2014. The germination strategies of widespread annual plants are unrelated to regional climate. Global Ecology and Biogeography 23: 1430-1439.
Miller-Rushing, A. J., T. T. Hoye, D. W. Inouye, and E. Post. 2010. The effects of phenological mismatches on demography. Philosophical Transactions of the Royal Society, B, Biological Sciences 365: 3177-3186.
Montesinos-Navarro, A., F. X. Pico, and S. J. Tonsor. 2012. Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana. Evolution 66: 3417-3431.
Murray, K., and M. M. Conner. 2009. Methods to quantify variable importance: implications for the analysis of noisy ecological data. Ecology 90: 348-355.
Ooi, M. K. J. 2012. Seed bank persistence and climate change. Seed Science Research 22: S53-S60.
Ooi, M. K. J., T. D. Auld, and A. J. Denham. 2009. Climate change and bet-hedging: interactions between increased soil temperatures and seed bank persistence. Global Change Biology 15: 2375-2386.
Parmesan, C., and M. E. Hanley. 2015. Plants and climate change: complexities and surprises. Annals of Botany 116: 849-864.
Penfield, S., and V. Springthorpe. 2012. Understanding chilling responses in Arabidopsis seeds and their contribution to life history. Philosophical Transactions of the Royal Society, B, Biological Sciences 367: 291-297.
Philippi, T. 1993. Bet-hedging germination of desert annuals: variation among populations and maternal effects in Lepidium lasiocarpum. American Naturalist 142: 488-507.
Philippi, T., and J. Seger. 1989. Hedging ones evolutionary bets, revisited. Trends in Ecology & Evolution 4: 41-44.
Picó, F. X. 2012. Demographic fate of Arabidopsis thaliana cohorts of autumn- and spring-germinated plants along an altitudinal gradient. Journal of Ecology 100: 1009-1018.
Preston, R. E. 1991. The intrafloral phenology of Streptanthus tortuosus (Brassicaceae). American Journal of Botany 78: 1044-1053.
PRISM Climate Group. 2004. PRISM climate data. Northwest Alliance for Computational Science & Engineering, Oregon State University, Corvallis, OR, USA. Available at http://prism.oregonstate.edu [accessed 01 May 2019].
Rubin, M. J., and J. Friedman. 2018. The role of cold cues at different life stages on germination and flowering phenology. American Journal of Botany 105: 749-759.
Rundel, P. W., M. T. K. Arroyo, R. M. Cowling, J. E. Keeley, B. B. Lamont, and P. Vargas. 2016. Mediterranean biomes: evolution of their vegetation, floras, and climate. Annual Review of Ecology, Evolution, and Systematics 47: 383-407.
Seger, J., and H. J. Brockmann. 1987. What is bet-hedging? Oxford Surveys in Evolutionary Biology 4: 182-211.
Sheth, S. N., and A. L. Angert. 2014. The evolution of environmental tolerance and range size: a comparison of geographically restricted and widespread Mimulus. Evolution 68: 2917-2931.
Shimono, Y., and G. Kudo. 2005. Comparisons of germination traits of alpine plants between fellfield and snowbed habitats. Ecological Research 20: 189-197.
Simons, A. M. 2011. Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proceedings of the Royal Society, B, Biological Sciences 278: 1601-1609.
Simons, A. M. 2014. Playing smart vs. playing safe: the joint expression of phenotypic plasticity and potential bet hedging across and within thermal environments. Journal of Evolutionary Biology 27: 1047-1056.
Springthorpe, V., and S. Penfield. 2015. Flowering time and seed dormancy control use external coincidence to generate life history strategy. eLife 4: e05557.
Tielborger, K., M. Petru, and C. Lampei. 2012. Bet-hedging germination in annual plants: a sound empirical test of the theoretical foundations. Oikos 121: 1860-1868.
Torres-Martínez, L., P. Weldy, M. Levy, and N. C. Emery. 2017. Spatiotemporal heterogeneity in precipitation patterns explain population-level germination strategies in an edaphic specialist. Annals of Botany 119: 253-265.
Tudela-Isanta, M., E. Fernández-Pascual, M. Wijayasinghe, S. Orsenigo, G. Rossi, H. W. Pritchard, and A. Mondoni. 2018. Habitat-related seed germination traits in alpine habitats. Ecology and Evolution 8: 150-161.
Venable, D. L. 2007. Bet hedging in a guild of desert annuals. Ecology 88: 1086-1090.
Venable, D. L., and L. Lawlor. 1980. Delayed germination and dispersal in desert annuals: escape in space and time. Oecologia 46: 272-282.
Vidigal, D. S., A. C. Marques, L. A. Willems, G. Buijs, B. Mendez-Vigo, H. W. Hilhorst, L. Bentsink, et al. 2016. Altitudinal and climatic associations of seed dormancy and flowering traits evidence adaptation of annual life cycle timing in Arabidopsis thaliana. Plant, Cell & Environment 39: 1737-1748.
Wadgymar, S. M., R. M. Mactavish, and J. T. Anderson. 2018. Transgenerational and within-generation plasticity in response to climate change: insights from a manipulative field experiment across an elevational gradient. American Naturalist 192: 698-714.
Walck, J. L., S. N. Hidayati, K. W. Dixon, K. E. N. Thompson, and P. Poschlod. 2011. Climate change and plant regeneration from seed. Global Change Biology 17: 2145-2161.
Wilczek, A. M., J. L. Roe, M. C. Knapp, M. D. Cooper, C. Lopez-Gallego, L. J. Martin, C. D. Muir, et al. 2009. Effects of genetic perturbation on seasonal life history plasticity. Science 323: 930-934.
Winkler, D. E., J. R. Gremer, K. J. Chapin, M. Kao, and T. E. Huxman. 2018. Rapid alignment of functional trait variation with locality across the invaded range of Sahara mustard (Brassica tournefortii). American Journal of Botany 105: 1188-1197.