Abstract
Spatial and temporal environmental variability can lead to variation in selection pressures across a landscape. Strategies for coping with environmental heterogeneity range from specialized phenotypic responses to a narrow range of conditions to generalist strategies that function under a range of conditions. Here, we ask how mean climate and climate variation at individual sites and across a species’ range affect the specialist-generalist spectrum of germination strategies exhibited by 10 arid land forbs. We investigated these relationships using climate data for the western United States, occurrence records from herbaria, and germination trials with field-collected seeds, and predicted that generalist strategies would be most common in species that experience a high degree of climate variation or occur over a wide range of conditions. We used two metrics to describe variation in germination strategies: (a) selectivity (did seeds require specific cues to germinate?) and (b) population-level variation (did populations differ in their responses to germination cues?) in germination displayed by each species. Species exhibited distinct germination strategies, with some species demonstrating as much among-population variation as we observed among species. Modeling efforts suggested that generalist strategies evolve in response to higher spatial variation in actual evapotranspiration at a local scale and in available water in the spring and annual precipitation at a range-wide scale. Describing the conditions that lead to variation in early life-history traits is important for understanding the evolution of diversity in natural systems, as well as the possible responses of individual species to global climate change.
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References
Abdi H (2010) Coefficient of variation. In: Salkind N (ed) Encyclopedia of research design. Sage, Thousand Oaks, pp 169–171
Adler PB, Hillerislambers J, Kyriakidis PC, Guan Q, Levine JM, Tilman GD (2006) Climate variability has a stabilizing effect on the coexistence of prairie grasses. Proc Natl Acadamy Sci 103:12793–12798. doi:10.1073/pnas.0600599103
Banta JA, Ehrenreich IM, Gerard S, Chou L, Wilczek A, Schmitt J, Kover PX, Purugganan MD (2012) Climate envelope modelling reveals intraspecific relationships among flowering phenology, niche breadth and potential range size in Arabidopsis thaliana. Ecol Lett 15:769–777. doi:10.1111/j.1461-0248.2012.01796.x
Barton K (2016) MuMIn: multi-model inference, v. 1.15.6. https://cran.r-project.org/package=MuMIn
Baskin JM, Baskin CC (1972) Influence of germination date on survival and seed production in a natural population of Leavenworthia stylosa. Am Midl Nat 88:318–323. doi:10.2307/2424357
Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination, 2nd edn. Academic Press, San Diego
Baskin CC, Thompson K, Baskin JM (2006) Mistakes in germination ecology and how to avoid them. Seed Sci Res 16:165–168. doi:10.1079/SSR2006247
Becker U, Dostal P, Jorritsma-Wienk LD, Matthies D (2008) The spatial scale of adaptive population differentiation in a wide-spread, well-dispersed plant species. Oikos 117:1865–1873. doi:10.1111/j.0030-1299.2008.16939.x
Bell G, Lechowicz MJ, Waterway MJ (2000) Environmental heterogeneity and species diversity of forest sedges. J Ecol 88:67–87. doi:10.1046/j.1365-2745.2000.00427.x
Booth TH, Searle SD, Boland DJ (1989) Bioclimatic analysis to assist provenance selection for trials. New For 3:225–234. doi:10.1007/BF00028930
Boria RA, Olson LE, Goodman SM, Anderson RP (2014) Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol Modell 275:73–77. doi:10.1016/j.ecolmodel.2013.12.012
Botero CA, Weissing FJ, Wright J, Rubenstein DR, Pacala SW (2015) Evolutionary tipping points in the capacity to adapt to environmental change. Proc Natl Acadamy Sci 112:184–189. doi:10.1073/pnas.1408589111
Bradshaw A (1965) The evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155. doi:10.1016/s0065-2660(08)60048-6
Brändle M, Stadler J, Klotz S, Brandl R (2003) Distributional range size of weedy plant species is correlated to germination patterns. Ecology 84:136–144. doi:10.1890/0012-9658(2003)084[0136:DRSOWP]2.0.CO;2
Brown JL (2014) SDMtoolbox: a python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol Evol 5:694–700. doi:10.1111/2041-210X.12200
Brown R, Mayer D (1988) Representing cumulative germination. 2. The use of the Weibull function and other empirically derived curves. Ann Bot 61:127–138. doi:10.1093/oxfordjournals.aob.a087535
Burnham K, Anderson D (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York
Carta A, Probert R, Puglia G, Peruzzi L, Bedini G (2016) Local climate explains degree of seed dormancy in Hypericum elodes L. (Hypericaceae). Plant Biol 18:76–82. doi:10.1111/plb.12310
Chesson P, Gebauer RLE, Schwinning S, Huntly N, Wiegand K, Ernest MSK, Sher A, Novoplansky A, Weltzin JF (2004) Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia 141:236–253. doi:10.1007/s00442-004-1551-1
Clauss MJ, Venable DL (2000) Seed germination in desert annuals: an empirical test of adaptive bet hedging. Am Nat 155:168–186. doi:10.1086/303314
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? Glob Ecol Biogeogr 24:12–24. doi:10.1111/geb.12234
Cohen D (1966) Optimizing reproduction in a randomly varying environment. J Theor Biol 12:119–129. doi:10.1016/0022-5193(66)90188-3
Comstock JP, Ehleringer JR (1992) Plant adaptations in the Great Basin and Colorado Plateau. Gt Basin Nat 52:195–215
Condon C, Cooper BS, Yeaman S, Angilletta MJ (2014) Temporal variation favors the evolution of generalists in experimental populations of Drosophila melanogaster. Evolution (N Y) 68:720–728. doi:10.1111/evo.12296
Cook SA, Johnson MP (1968) Adaptation to heterogeneous environments. I. Variation in heterophylly in Ranunculus flammula L. Evolution (N Y) 22:496–516. doi:10.1111/j.1558-5646.1968.tb03988.x
Daly C, Halbleib M, Smith JI, Gibson WP, Doggett MK, Taylor GH, Curtis J, Pasteris PP (2008) Physiographically sensitive mapping of climatological temperature and precipitation across the conterminous United States. Int J Climatol 28:2031–2064. doi:10.1002/joc.1688
Dilts TE, Weisberg PJ, Dencker CM, Chambers JC (2015) Functionally relevant climate variables for arid lands: a climatic water deficit approach for modelling desert shrub distributions. J Biogeogr 42:1986–1997. doi:10.1111/jbi.12561
Doherty KD, Butterfield BJ, Wood TE (2017) Matching seed to site by climate similarity: techniques to prioritize plant materials development and use in restoration. Ecol Appl. doi:10.1002/eap.1505
Donohue K, Dorn L, Griffith C, Kim E, Aguilera A, Polisetty CR, Schmitt J (2005) The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution (N Y) 59:758–770. doi:10.1111/j.0014-3820.2005.tb01751.x
Donohue K, Rubio De Casas R, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319. doi:10.1146/annurev-ecolsys-102209-144715
Ellner S (1985) ESS germination strategies in randomly varying environments. I. Logistic-type models. Theor Popul Biol 28:50–79. doi:10.1016/0040-5809(85)90022-x
Forbis TA (2010) Germination phenology of some Great Basin native annual forb species. Plant Species Biol 25:221–230. doi:10.1111/j.1442-1984.2010.00289.x
Fraaije RGA, ter Braak CJF, Verduyn B, Breeman LBS, Verhoeven JTA, Soons MB (2015) Early plant recruitment stages set the template for the development of vegetation patterns along a hydrological gradient. Funct Ecol 29:971–980. doi:10.1111/1365-2435.12441
Freas KE, Kemp PR (1983) Some relationships between environmental reliability and seed dormancy in desert annual plants. J Ecol 71:211–217. doi:10.2307/2259973
Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233. doi:10.1146/annurev.ecolsys.19.1.207
Gabriel W, Luttbeg B, Sih A, Tollrian R (2005) Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am Nat 166:339–353. doi:10.1086/432558
Granado-Yela C, Balaguer L, García-Verdugo C, Carrillo K, Méndez M (2013) Thriving at the limit: differential reproductive performance in range-edge populations of a Mediterranean sclerophyll (Olea europaea). Acta Oecologica 52:29–37. doi:10.1016/j.actao.2013.07.002
Gremer JR, Kimball S, Venable DL, Pannell J (2016) Within-and among-year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment. Ecol Lett 19:1209–1218. doi:10.1111/ele.12655
Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711. doi:10.1111/j.1420-9101.2010.02210.x
Gutterman Y (2000) Maternal effects on seeds during development. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI Publishing, Wallingford, pp 59–84
Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588. doi:10.1086/597611
Heschel MS, Sultan SE, Glover S, Sloan D (2004) Population differentiation and plastic responses to drought stress in the generalist annual Polygonum persicaria. Int J Plant Sci 165:817–824. doi:10.1086/421477
Jiménez-Alfaro B, Silveira FAO, Fidelis A, Poschlod P, Commander LE (2016) Seed germination traits can contribute better to plant community ecology. J Veg Sci 27:637–645. doi:10.1111/jvs.12375
Kadmon R, Shmida A (1990) Competition in a variable environment: an experimental study in a desert annual plant population. Isr J Bot 39:403–412
Kassen R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15:173–190. doi:10.1046/j.1420-9101.2002.00377.x
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi:10.1111/j.1461-0248.2004.00684.x
Kos M, Poschlod P (2007) Seeds use temperature cues to ensure germination under nurse-plant shade in xeric Kalahari savannah. Ann Bot 99:667–675. doi:10.1093/aob/mcl293
Kramer-Schadt S, Niedballa J, Pilgrim JD, Schröder B, Lindenborn J, Reinfelder V, Stillfried M, Heckmann I, Scharf AK, Augeri DM, Cheyne SM, Hearn AJ, Ross J, Macdonald DW, Mathai J, Eaton J, Marshall AJ, Semiadi G, Rustam R, Bernard H, Alfred R, Samejima H, Duckworth JW, Breitenmoser-Wuersten C, Belant JL, Hofer H, Wilting A (2013) The importance of correcting for sampling bias in MaxEnt species distribution models. Divers Distrib 19:1366–1379. doi:10.1111/ddi.12096
Kulpa SM, Leger EA (2013) Strong natural selection during plant restoration favors an unexpected suite of plant traits. Evol Appl 6:510–523. doi:10.1111/eva.12038
Lechowicz MJ, Bell G (1991) The ecology and genetics of fitness in forest plants. II. Microspatial heterogeneity of the edaphic environment. J Ecol 79:687–696. doi:10.2307/2260661
Leger EA, Espeland EK, Merrill KR, Meyer SE (2009) Genetic variation and local adaptation at a cheatgrass (Bromus tectorum) invasion edge in western Nevada. Mol Ecol 18:4366–4379. doi:10.1111/j.1365-294X.2009.04357.x
Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS ONE 3:1–8. doi:10.1371/journal.pone.0004010
Levine JM, Rees M (2004) Effects of temporal variability on rare plant persistence in annual systems. Am Nat 164:350–363. doi:10.1086/422859
Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in p lants. Annu Rev Ecol Syst 27:237–277. doi:10.1146/annurev.ecolsys.27.1.237
Luna B, Pérez B, Torres I, Moreno JM (2012) Effects of Incubation temperature on seed germination of Mediterranean plants with different geographical distribution ranges. Folia Geobot 47:17–27. doi:10.1007/s12224-011-9110-0
Lutz JA, Van Wagtendonk JW, Franklin JF (2010) Climatic water deficit, tree species ranges, and climate change in Yosemite National Park. J Biogeogr 37:936–950. doi:10.1111/j.1365-2699.2009.02268.x
Macel M, Lawson CS, Mortimer SR, Šmilauerova M, Bischoff A, Crémieux L, Doleźal J, Edwards AR, Lanta V, Bezemer TM, Van Der Putten WH, Igual JM, Rodriguez-Barrueco C, Müller-Schärer H, Steinger T (2007) Climate vs. soil factors in local adaptation of two common plant species. Ecology 88:424–433. doi:10.1890/0012-9658(2007)88[424:CVSFIL]2.0.CO;2
Marks M, Prince S (1981) Influence of germination date on survival and fecundity in wild lettuce Lactuca serriola. Oikos 36:326–330. doi:10.2307/3544630
Menges ES (1991) Seed germination percentage increases with population size in a fragmented prairie species. Conserv Biol 5:158–164. doi:10.1111/j.1523-1739.1991.tb00120.x
Meyer SE, Kitchen SG, Carlson SL (1995) Seed germination timing patterns in Intermountain Penstemon (Scrophulariaceae). Am J Bot 82:377–389. doi:10.2307/2445584
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. doi:10.1093/aob/mcv101
Moreira B, Tavsanoglu C, Pausas J (2012) Local versus regional intraspecific variability in regeneration traits. Oecologia 168:671–677. doi:10.1007/S00442-01
Nagy ES, Rice KJ (1997) Local adaptation in two subspecies of an annual plant: implications for migration and gene flow. Evolution (N Y) 51:1079–1089. doi:10.2307/2411037
Nevoux M, Forcada J, Barbraud C, Croxall J, Weimerskirch H (2010) Bet-hedging response to environmental variability, an intraspecific comparison. Ecology 91:2416–2427. doi:10.1890/09-0143.1
Pake CE, Venable DL (1996) Seed banks in desert annuals: implications for persistence and coexistence in variable environments. Ecology 77:1427–1435. doi:10.2307/2265540
Petru M, Tielborger K (2008) Germination behaviour of annual plants under changing climatic conditions: separating local and regional environmental effects. Oecologia 155:717–728. doi:10.1007/s00442-007-0955-0
Poschlod P, Abedi M, Bartelheimer M, Drobnik J, Rosbakh S, Saatkamp A (2013) Seed ecology and assembly rules in plant communities. In: van der Maarel E, Franklin J (eds) Vegetation Ecology, 2nd edn. Wiley, Chichester, pp 164–202
Prendeville HR, Barnard-Kubow K, Dai C, Barringer BC, Galloway LF (2013) Clinal variation for only some phenological traits across a species range. Oecologia 173:421–430. doi:10.1007/s00442-013-2630-y
R Development Core Team (2016) R: A language and environment for statistical computing. R http://www.r-project.org/. Vienna, Austria
Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214. doi:10.1146/annurev.es.16.110185.001143
Raynal DJ, Bazzaz FA (1975) Interference of winter annuals with Ambrosia artemisiifolia in early successional fields. Ecology 56:35–49. doi:10.2307/1935298
Reboud X, Bell G (1997) Experimental evolution in Chlamydomonas. Ill. Evolution of specialist and generalist types in environments that vary in space and time. Heredity (Edinb) 78:507–514. doi:10.1038/sj.hdy.6881210
Rosbakh S, Poschlod P (2015) Initial temperature of seed germination as related to species occurrence along a temperature gradient. Funct Ecol 29:5–14. doi:10.1111/1365-2435.12304
Sambatti JBM, Rice KJ (2006) Local adaptation, patterns of selection, and gene flow in the California serpentine sunflower (Helianthus exilis). Evolution (N Y) 60:696–710. doi:10.1554/05-479.1
Santamaria L, Figuerola J, Pilon JJ, Mjelde M, Green AJ, De Boer T, King RA, Gornall RJ (2003) Plant performance across latitude: the role of plasticity and local adaptation in an aquatic plant. Ecology 84:2454–2461. doi:10.1890/02-0431
Schwinning S, Sala OE, Loik ME, Ehleringer JR (2004) Thresholds, memory, and seasonality: understanding pulse dynamics in arid/semi-arid ecosystems. Oecologia 141:191–193. doi:10.1007/s00442-004-1683-3
Sher AA, Goldberg DE, Novoplansky A (2004) The effect of mean and variance in resource supply on survival of annuals from Mediterranean and desert environments. Oecologia 141:353–362. doi:10.1007/s00442-003-1435-9
Simons AM (2014) Playing smart vs. playing safe: the joint expression of phenotypic plasticity and potential bet hedging across and within thermal environments. J Evol Biol 27:1047–1056. doi:10.1111/jeb.12378
Snaydon RW, Davies TM (1982) Rapid divergence of plant populations in response to recent changes in soil conditions. Source Evol 36:289–297. doi:10.2307/2408047
Stephenson NL (1998) Actual evapotranspiration and deficit: biologically meaningful correlates of vegetation distribution across spatial scales. J Biogeogr 25:855–870. doi:10.1046/j.1365-2699.1998.00233.x
Sultan SE (1987) DNA evolutionary implications of phenotypic plasticity in plants. In: Hecht MK, Wallace B, Prance GT (eds) Evolutionary biology, vol 21. Springer, New York, pp 127–178
Sultan SE (2000) Phenotypic plasticity for plant development, function, and life history. Trends Plant Sci 5:537–542. doi:10.1016/s1360-1385(00)01797-0
Therneau TM (2015) A package for survival analysis in S, v. 2.38. https://cran.r-project.org/package=survival
Torres-Martinez L, Weldy P, Levy M, Emery NC (2016) Spatiotemporal heterogeneity in precipitation patterns explain population-level germination strategies in an edaphic specialist. Ann Bot 1–13:253–265. doi:10.1093/aob/mcw161
Treurnicht M, Pagel J, Esler KJ, Schutte-Vlok A, Nottebrock H, Kraaij T, Rebelo AG, Schurr FM (2016) Environmental drivers of demographic variation across the global geographical range of 26 plant species. J Ecol 104:331–342. doi:10.1111/1365-2745.12508
Turkington R, Harper JL (1979) The growth, distribution and neighbour relationships of Trifolium repens in a permanent pasture: IV. Fine-scale biotic differentiation. J Ecol 67:245–254. doi:10.2307/2259348
Valladares F, Gianoli E, Gomez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763. doi:10.1111/j.1469-8137.2007.02275.x
Venable DL (2007) Bet hedging in a guild of desert annuals. Ecology 88:1086–1090. doi:10.1890/06-1495
Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217. doi:10.1016/s0169-5347(00)89061-8
Warwick SI, Briggs D (1978) The genecology of lawn weeds: II. Evidence for disruptive selection in Poa annua L. in a mosaic environment of bowling green lawns and flower bedsI. New Phytol 81:725–737. doi:10.1111/j.1469-8137.1978.tb01647.x
Weaver SE, Cavers PB (1979) The effects of date of emergence and emergence order on seedling survival rates in Rumex crispus and R. obtusifolius. Can J Bot 57:730–738. doi:10.1139/b79-092
Weinig C (2000) Differing selection in alternative competition environments: shade-avoidance responses and germination timing. Evolution (N Y) 54:124–136. doi:10.1111/j.0014-3820.2000.tb00013.x
Winsor J (1983) Persistence by habitat dominance in the annual Impatiens capensis (Balsaminaceae). J Ecol 71:451–466. doi:10.2307/2259727
Wright JW, Stanton ML, Scherson R (2006) Local adaptation to serpentine and non-serpentine soils in Collinsia sparsiflora. Evol Ecol Res 8:1–21
Acknowledgements
We would like to thank the Great Basin Native Plant Project for their generous funding and the Germplasm Research Information Network/National Plant Germplasm System (GRIN/NPGS) for providing me with hand-collected seeds for my work with Phacelia hastata. Brittany Trimble, Lyndsey Boyer, Travis Allen, Vicki Thill, and Brianna Koorman provided valuable assistance with seed germination monitoring.
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SCB and EAL conceived and designed the experiments. SCB performed the germination experiments. TED generated climate data and assisted with analyses using geospatial information and tools. SCB analyzed the data. SCB and EAL wrote the manuscript, and TED edited the manuscript.
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Barga, S., Dilts, T.E. & Leger, E.A. Climate variability affects the germination strategies exhibited by arid land plants. Oecologia 185, 437–452 (2017). https://doi.org/10.1007/s00442-017-3958-5
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DOI: https://doi.org/10.1007/s00442-017-3958-5