Abstract
Understanding the resistance and resilience of foundation plant species to climate change is a critical issue because the loss of these species would fundamentally reshape communities and ecosystem processes. High levels of population genetic diversity may buffer foundation species against climate disruptions, but the strong selective pressures associated with climatic shifts may also rapidly reduce such diversity. We characterized genetic diversity and its responsiveness to experimental drought in the foundation plant, black grama grass (Bouteloua eriopoda), which dominates many western North American grasslands and shrublands. Previous studies suggested that in arid ecosystems, black grama reproduces largely asexually via stolons, and thus is likely to have low genetic variability, which might limit its potential to respond to climate disruptions. Using genotyping-by-sequencing, we demonstrated unexpectedly high genetic variability among black grama plants in a 1 ha site within the Sevilleta National Wildlife Refuge in central New Mexico, suggesting some level of sexual reproduction. Three years of experimental, growing season drought reduced black grama survival and biomass (the latter by 96%), with clear genetic differentiation (higher FST) between plants succumbing to drought and those remaining alive. Reduced genetic variability in the surviving plants in drought plots indicated that the experimental drought had forced black grama populations through selection bottlenecks. These results suggest that foundation grass species, such as black grama, may experience rapid evolutionary change if future climates include more severe droughts.
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Ahlstrom A, Raupach MR, Schurgers G, Smith B, Arneth A, Jung M, Reichstein M, Canadell JG, Friedlingstein P, Jain AK, Kato E, Poulter B, Sitch S, Stocker BD, Viovy N, Wang YP, Wiltshire A, Zaehle S, Zeng N (2015) The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science 348:895–899. https://doi.org/10.1126/science.aaa1668
Anand S, Mangano E, Barizzone N, Bordoni R, Sorosina M, Clarelli F, Corrado L, Boneschi FM, D'Alfonso S, De Bellis G (2016) Next generation sequencing of pooled samples: guideline for variants' filtering. Sci Rep. https://doi.org/10.1038/srep33735
Anderson JT (2016) Plant fitness in a rapidly changing world. New Phytol 210:81–87. https://doi.org/10.1111/nph.13693
Atwater DZ, Callaway RM (2015) Testing the mechanisms of diversity-dependent overyielding in a grass species. Ecology 96:3332–3342. https://doi.org/10.1890/15-0889.1
Avolio ML, Beaulieu JM, Smith MD (2013) Genetic diversity of a dominant C-4 grass is altered with increased precipitation variability. Oecologia 171:571–581. https://doi.org/10.1007/s00442-012-2427-4
Avolio ML, Smith MD (2013) Mechanisms of selection: phenotypic differences among genotypes explain patterns of selection in a dominant species. Ecology 94:953–965
Báez S, Collins SL, Pockman WT, Johnson JE, Small EE (2013) Effects of experimental rainfall manipulations on Chihuahuan Desert grassland and shrubland plant communities. Oecologia 172:1117–1127. https://doi.org/10.1007/s00442-012-2552-0
Báez S, Collins SL (2008) Shrub invasion decreases diversity and alters community stability in northern Chihuahuan Desert plant communities. PLoS One 3:e2332. https://doi.org/10.1371/journal.pone.0002332
Bangert RK, Lonsdorf EV, Wimp GM, Shuster SM, Fischer D, Schweitzer JA, Allan GJ, Bailey JK, Whitham TG (2008) Genetic structure of a foundation species: scaling community phenotypes from the individual to the region. Heredity 100:121–131. https://doi.org/10.1038/sj.hdy.6800914
Bates D, Maechler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Carroll SP, Jorgensen PS, Kinnison MT, Bergstrom CT, Denison RF, Gluckman P, Smith TB, Strauss SY, Tabashnik BE (2014) Applying evolutionary biology to address global challenges. Science 346:313. https://doi.org/10.1126/science.1245993
Collins SL, Xia Y (2015) Long-term dynamics and hotspots of change in a desert grassland plant community. Am Nat 185:E30–E43. https://doi.org/10.1086/679315
Connin SL, Virginia RA, Chamberlain CP (1997) Carbon isotopes reveal soil organic matter dynamics following arid land shrub expansion. Oecologia 110:374–386. https://doi.org/10.1007/s004420050172
Cook BI, Ault TR, Smerdon JE (2015) Unprecedented 21st century drought risk in the American Southwest and Central Plains. Sci Adv. https://doi.org/10.1126/sciadv.1400082
Cook-Patton SC, McArt SH, Parachnowitsch AL, Thaler JS, Agrawal AA (2011) A direct comparison of the consequences of plant genotypic and species diversity on communities and ecosystem function. Ecology 92:915–923. https://doi.org/10.1890/10-0999.1
Cox JR, Martin MH, Ibarra FA, Morton HL (1986) Establishment of range grasses on various seedbeds at creosotebush Larrea tridentata sites in Arizona, USA, and Chihuahua, Mexico. J Range Manag 39:540–546. https://doi.org/10.2307/3898767
Crawford KM, Rudgers JA (2012) Plant species diversity and genetic diversity within a dominant species interactively affect plant community biomass. J Ecol 100:1512–1521. https://doi.org/10.1111/j.1365-2745.2012.02016.x
Crawford KM, Whitney KD (2010) Population genetic diversity influences colonization success. Mol Ecol 19:1253–1263
Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968. https://doi.org/10.1126/science.1128326
Dick-Peddie WA (1993) New Mexico vegetation: past, present, and future. University of New Mexico Press, Albuquerque
Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, Von Holle B, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486. https://doi.org/10.1890/1540-9295(2005)003[0479:LOFSCF]2.0.CO;2
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. https://doi.org/10.1371/journal.pone.0019379
Fox JW (2005) Interpreting the 'selection effect' of biodiversity on ecosystem function. Ecol Lett 8:846–856. https://doi.org/10.1111/j.1461-0248.2005.00795.x
Fracassetti M, Griffin PC, Willi Y (2015) Validation of pooled whole-genome re-sequencing in Arabidopsis lyrata. PLoS One. https://doi.org/10.1371/journal.pone.0140462
Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc Nat Acad Sci USA 104:1278–1282
Franks SJ, Weber JJ, Aitken SN (2014) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol Appl 7:123–139. https://doi.org/10.1111/eva.12112
Franks SJ, Kane NC, O'Hara NB, Tittes S, Rest JS (2016) Rapid genome-wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools. Mol Ecol 25:3622–3631. https://doi.org/10.1111/mec.13615
Garfin G, Franco G, Blanco H, Comrie A, Gonzalez P, Piechota T, Smyth R, Waskom R (2014) Chapter 20: Southwest. In: Melillo JM, Richmond TC, Yohe GW (eds) Climate change impacts in the United States: the third national climate assessment. U.S Global Change Research Program, Washington, pp 462–486
Gautier M, Foucaud J, Gharbi K, Cezard T, Galan M, Loiseau A, Thomson M, Pudlo P, Kerdelhue C, Estoup A (2013) Estimation of population allele frequencies from next-generation sequencing data: pool-versus individual-based genotyping. Mol Ecol 22:3766–3779. https://doi.org/10.1111/mec.12360
Gogarten SM, Zheng X (2017) SeqVarTools: tools for variant data. R package version 1.8.1, R package version 1.8.1 edn
Gosz RJ, Gosz JR (1996) Species interactions on the biome transition zone in New Mexico: response of blue grama (Bouteloua gracilis) and black grama (Bouteloua eripoda) to fire and herbivory. J Arid Environ 34:101–114. https://doi.org/10.1006/jare.1996.0096
Gould F (1979) The genus Bouteloua (Poaceae). Ann Mo Bot Gard 66:348–416. https://doi.org/10.2307/2398834
Hart SP, Schreiber SJ, Levine JM (2016) How variation between individuals affects species coexistence. Ecol Lett 19:825–838. https://doi.org/10.1111/ele.12618
Huang JP, Ji MX, Xie YK, Wang SS, He YL, Ran JJ (2016a) Global semi-arid climate change over last 60 years. Clim Dyn 46:1131–1150. https://doi.org/10.1007/s00382-015-2636-8
Huang JP, Yu HP, Guan XD, Wang GY, Guo RX (2016b) Accelerated dryland expansion under climate change. Nat Clim Change 6:166. https://doi.org/10.1038/nclimate2837
Huber H, During HJ, de Bruin FB, Vermeulen PJ, Anten NPR (2016) Genotypic and phenotypic diversity does not affect productivity and drought response in competitive stands of Trifolium repens. Front Plant Sci 7:364. https://doi.org/10.3389/fpls.2016.00364
Huenneke LF, Clason D, Muldavin E (2001) Spatial heterogeneity in Chihuahuan Desert vegetation: implications for sampling methods in semi-arid ecosystems. J Arid Environ 47:257–270. https://doi.org/10.1006/jare.2000.0678
Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623. https://doi.org/10.1111/j.1461-0248.2008.01179.x
Ikeda DH, Max TL, Allan GJ, Lau MK, Shuster SM, Whitham TG (2017) Genetically informed ecological niche models improve climate change predictions. Glob Change Biol 23:164–176. https://doi.org/10.1111/gcb.13470
IPCC (2013) Climate change 2013: the physical science basis. Fifth assessment report of the intergovernmental panel on climate change. Cambridge Press, New York
Isbell F, Craven D, Connolly J, Loreau M, Schmid B, Beierkuhnlein C, Bezemer TM, Bonin C, Bruelheide H, de Luca E, Ebeling A, Griffin JN, Guo QF, Hautier Y, Hector A, Jentsch A, Kreyling J, Lanta V, Manning P, Meyer ST, Mori AS, Naeem S, Niklaus PA, Polley HW, Reich PB, Roscher C, Seabloom EW, Smith MD, Thakur MP, Tilman D, Tracy BF, van der Putten WH, van Ruijven J, Weigelt A, Weisser WW, Wilsey B, Eisenhauer N (2015) Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526:574–U263. https://doi.org/10.1038/nature15374
Jimenez-Alfaro B, Garcia-Calvo L, Garcia P, Luis Acebes J (2016) Anticipating extinctions of glacial relict populations in mountain refugia. Biol Conserv 201:243–251. https://doi.org/10.1016/j.biocon.2016.07.015
Jump AS, Penuelas J, Rico L, Ramallo E, Estiarte M, Martinez-Izquierdo JA, Lloret F (2008) Simulated climate change provokes rapid genetic change in the Mediterranean shrub Fumana thymifolia. Glob Change Biol 14:637–643. https://doi.org/10.1111/j.1365-2486.2007.01521.x
Jump AS, Marchant R, Penuelas J (2009) Environmental change and the option value of genetic diversity. Trends Plant Sci 14:51–58. https://doi.org/10.1016/j.tplants.2008.10.002
Knapp AK, Hoover DL, Wilcox KR, Avolio ML, Koerner SE, La Pierre KJ, Loik ME, Luo YQ, Sala OE, Smith MD (2015) Characterizing differences in precipitation regimes of extreme wet and dry years: implications for climate change experiments. Glob Change Biol 21:2624–2633. https://doi.org/10.1111/gcb.12888
Knapp AK, Avolio ML, Beier C, Carroll CJW, Collins SL, Dukes JS, Fraser LH, Griffin-Nolan RJ, Hoover DL, Jentsch A, Loik ME, Phillips RP, Post AK, Sala OE, Slette IJ, Yahdjian L, Smith MD (2017) Pushing precipitation to the extremes in distributed experiments: recommendations for simulating wet and dry years. Glob Change Biol 23:1774–1782. https://doi.org/10.1111/gcb.13504
Kofler R, Nolte V, Schloetterer C (2016) The impact of library preparation protocols on the consistency of allele frequency estimates in Pool-Seq data. Mol Ecol Res 16:118–122. https://doi.org/10.1111/1755-0998.12432
Latzel V, Allan E, Silveira AB, Colot V, Fischer M, Bossdorf O (2013) Epigenetic diversity increases the productivity and stability of plant populations. Nat Commun 4:UNSP-2875. https://doi.org/10.1038/ncomms3875
Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Nat Acad Sci USA 109:14058–14062. https://doi.org/10.1073/pnas.1202319109
Lauenroth WK, Adler PB (2008) Demography of perennial grassland plants: survival, life expectancy and life span. J Ecol 96:1023–1032. https://doi.org/10.1111/j.1365-2745.2008.01415.x
Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9:e1003215. https://doi.org/10.1371/journal.pgen.1003215
Lucero ME, Dreesen DR, VanLeeuwen DM (2010) Using hydrogel filled, embedded tubes to sustain grass transplants for arid land restoration. J Arid Environ 74:987–990. https://doi.org/10.1016/j.jaridenv.2010.01.007
Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Gen 4:981–994. https://doi.org/10.1038/nrg1226
Lynch M, Bost D, Wilson S, Maruki T, Harrison S (2014) Population-genetic inference from pooled-sequencing data. Genome Biol Evol 6:1210–1218. https://doi.org/10.1093/gbe/evu085
McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185. https://doi.org/10.1016/j.tree.2006.02.002
McManus CJ, Kelley ST (2005) Molecular survey of aeroplane bacterial contamination. J Appl Microbiol 99:502–508. https://doi.org/10.1111/j.1365-2672.2005.02651.x
Medrano M, Herrera CM, Bazaga P (2014) Epigenetic variation predicts regional and local intraspecific functional diversity in a perennial herb. Mol Ecol 23:4926–4938. https://doi.org/10.1111/mec.12911
Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14. https://doi.org/10.1111/eva.12137
Milla R, Forero DM, Escudero A, Iriondo JM (2009) Growing with siblings: a common ground for cooperation or for fiercer competition among plants? Proc R Soc B Biol Sci 276:2531–2540. https://doi.org/10.1098/rspb.2009.0369
Moreira X, Abdala-Roberts L, Parra-Tabla V, Mooney KA (2014) Positive effects of plant genotypic and species diversity on anti-herbivore defenses in a tropical tree species. PLoS One 9:e105438. https://doi.org/10.1371/journal.pone.0105438
Moreno-de las Heras M, Turnbull L, Wainwright J (2016) Seed-bank structure and plant-recruitment conditions regulate the dynamics of a grassland-shrubland Chihuahuan ecotone. Ecology 97:2303–2318. https://doi.org/10.1002/ecy.1446
Muldavin EH, Moore DI, Collins SL, Wetherill KR, Lightfoot DC (2008) Aboveground net primary production dynamics in a northern Chihuahuan Desert ecosystem. Oecologia 155:123–132. https://doi.org/10.1007/s00442-007-0880-2
Nevo E, Fu Y-B, Pavlicek T, Khalifa S, Tavasi M, Beiles A (2012) Evolution of wild cereals during 28 years of global warming in Israel. Proc Nat Acad Sci USA 109:3412–3415. https://doi.org/10.1073/pnas.1121411109
Nichol AA (1952) The natural vegetation of Arizona [revisions by Phillips, W. S.], Tucson, pp 189–230
Notaro M, Liu ZY, Gallimore RG, Williams JW, Gutzler DS, Collins S (2010j) Complex seasonal cycle of ecohydrology in the Southwest United States. J Geophys Res Biogeosci. https://doi.org/10.1029/2010jg001382
Ogle K, Barber JJ, Barron-Gafford GA, Bentley LP, Young JM, Huxman TE, Loik ME, Tissue DT (2015) Quantifying ecological memory in plant and ecosystem processes. Ecol Lett 18:221–235. https://doi.org/10.1111/ele.12399
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) vegan: community ecology package. R package version 2.3-5. https://CRAN.R-project.org/package=vegan. Accessed 1 Nov 2017
Parmenter RR (2008) Long-term effects of a summer fire on desert grassland plant demographics in now Mexico. Rangeland Ecol Manag 61:156–168. https://doi.org/10.2111/07-010.1
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Syst 37:637–669
Pauls SU, Nowak C, Balint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946. https://doi.org/10.1111/mec.12152
Paulsen HA Jr, Ares FN (1962) Grazing values and management of black grama and tobosa grasslands and associated shrub ranges of the Southwest. Department of Agriculture, Forest Service, Washington, DC, p 56
Peters DPC (2002) Recruitment potential of two perennial grasses with different growth forms at a semiarid-arid transition zone. Am J Bot 89:1616–1623. https://doi.org/10.3732/ajb.89.10.1616
Peters DPC, Mariotto I, Havstad KM, Murray LW (2006) Spatial variation in remnant grasses after a grassland-to-shrubland state change: implications for restoration. Rangeland Ecol Manag 59:343–350. https://doi.org/10.2111/05-202R1.1
Peters DPC, Herrick JE, Monger HC, Huang H (2010) Soil–vegetation–climate interactions in arid landscapes: effects of the North American monsoon on grass recruitment. J Arid Environ 74:618–623. https://doi.org/10.1016/j.jaridenv.2009.09.015
Peters DPC, Yao J (2012) Long-term experimental loss of foundation species: consequences for dynamics at ecotones across heterogeneous landscapes. Ecosphere 3:UNSP-27. https://doi.org/10.1890/ES11-00273.1
Pfeiffer F, Groeber C, Blank M, Haendler K, Beyer M, Schultze JL, Mayer G (2018) Systematic evaluation of error rates and causes in short samples in next-generation sequencing. Sci Rep. https://doi.org/10.1038/s41598-018-29325-6
Potvin C, Tousignant D (1996) Evolutionary consequences of simulated global change: genetic adaptation or adaptive phenotypic plasticity. Oecologia 108:683–693. https://doi.org/10.1007/BF00329043
Prati D, Peintinger M, Fischer M (2016) Genetic composition, genetic diversity and small-scale environmental variation matter for the experimental reintroduction of a rare plant. J Plant Ecol 9:805–813. https://doi.org/10.1093/jpe/rtv067
Pravalie R (2016) Drylands extent and environmental issues. A global approach. Earth Sci Rev 161:259–278. https://doi.org/10.1016/j.earscirev.2016.08.003
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ravenscroft CH, Whitlock R, Fridley JD (2015) Rapid genetic divergence in response to 15 years of simulated climate change. Glob Change Biol 21:4165–4176. https://doi.org/10.1111/gcb.12966
Reynolds HG, Bohning JW (1956) Effects of burning on a desert grass-shrub range in southern Arizona. Ecology 37:769–777. https://doi.org/10.2307/1933068
Rico L, Ogaya R, Barbeta A, Penuelas J (2014) Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change. Plant Biol 16:419–427. https://doi.org/10.1111/plb.12049
Rubidge EM, Patton JL, Lim M, Burton AC, Brashares JS, Moritz C (2012) Climate-induced range contraction drives genetic erosion in an alpine mammal. Nat Clim Change 2:285–288. https://doi.org/10.1038/NCLIMATE1415
Rudgers JA, Chung YA, Maurer GE, Moore DI, Muldavin EH, Litvak ME, Collins SL (2018) Climate sensitivity functions and net primary production: a framework for incorporating climate mean and variability. Ecology 99:576–582. https://doi.org/10.1002/ecy.2136
Schloetterer C, Tobler R, Kofler R, Nolte V (2014) Sequencing pools of individuals-mining genome-wide polymorphism data without big funding. Nat Rev Gen 15:749–763. https://doi.org/10.1038/nrg3803
Schoeb C, Kerle S, Karley AJ, Morcillo L, Pakeman RJ, Newton AC, Brooker RW (2015) Intraspecific genetic diversity and composition modify species-level diversity-productivity relationships. New Phytol 205:720–730. https://doi.org/10.1111/nph.13043
Shi Z, Thomey ML, Mowll W, Litvak M, Brunsell NA, Collins SL, Pockman WT, Smith MD, Knapp AK, Luo Y (2014) Differential effects of extreme drought on production and respiration: synthesis and modeling analysis. Biogeosciences 11:621–633. https://doi.org/10.5194/bg-11-621-2014
Siefert A, Violle C, Chalmandrier L, Albert CH, Taudiere A, Fajardo A, Aarssen LW, Baraloto C, Carlucci MB, Cianciaruso MV, Dantas VdL, de Bello F, Duarte LDS, Fonseca CR, Freschet GT, Gaucherand S, Gross N, Hikosaka K, Jackson B, Jung V, Kamiyama C, Katabuchi M, Kembel SW, Kichenin E, Kraft NJB, Lagerstrom A, Le Bagousse-Pinguet Y, Li Y, Mason N, Messier J, Nakashizuka T, McC Overton J, Peltzer DA, Perez-Ramos IM, Pillar VD, Prentice HC, Richardson S, Sasaki T, Schamp BS, Schoeb C, Shipley B, Sundqvist M, Sykes MT, Vandewalle M, Wardle DA (2015) A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecol Lett 18:1406–1419. https://doi.org/10.1111/ele.12508
Simonin KA (2000) Bouteloua eriopoda. In: Fire effects information system, [Online]. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory
Slowikowski K (2016) ggrepel: repulsive text and label geoms for 'ggplot2'. R package version 0.5, R package version 0.5. edn
Streetman LJ, Wright N (1960) A cytological study of black gramagrass Bouteloua eriopoda. Am J Bot 47:786–793. https://doi.org/10.2307/2439116
Thomey ML, Collins SL, Vargas R, Johnson JE, Brown RF, Natvig DO, Friggens MT (2011) Effect of precipitation variability on net primary production and soil respiration in a Chihuahuan Desert grassland. Glob Change Biol 17:1505–1515. https://doi.org/10.1111/j.1365-2486.2010.02363.x
Travers SE, Tang ZW, Caragea D, Garrett KA, Hulbert SH, Leach JE, Bai JF, Saleh A, Knapp AK, Fay PA, Nippert J, Schnable PS, Smith MD (2010) Variation in gene expression of Andropogon gerardii in response to altered environmental conditions associated with climate change. J Ecol 98:374–383. https://doi.org/10.1111/j.1365-2745.2009.01618.x
Valentine KA (1970) Influence of grazing intensity on improvement of deteriorated black grama range. Bulletin 553. New Mexico State University Agricultural Experiment Station, Las Cruces
Van Auken OW (2000) Shrub invasions of North American semiarid grasslands. Annu Rev Ecol Syst 31:197–215. https://doi.org/10.1146/annurev.ecolsys.31.1.197
Whitlock R (2014) Relationships between adaptive and neutral genetic diversity and ecological structure and functioning: a meta-analysis. J Ecol 102:857–872. https://doi.org/10.1111/1365-2745.12240
Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer, New York
Williams AP, Allen CD, Macalady AK, Griffin D, Woodhouse CA, Meko DM, Swetnam TW, Rauscher SA, Seager R, Grissino-Mayer HD, Dean JS, Cook ER, Gangodagamage C, Cai M, McDowell NG (2013) Temperature as a potent driver of regional forest drought stress and tree mortality. Nat Clim Change 3:292–297. https://doi.org/10.1038/nclimate1693
Yahdjian L, Sala OE (2002) A rainout shelter design for intercepting different amounts of rainfall. Oecologia 133:95–101. https://doi.org/10.1007/s00442-002-1024-3
Yang L, Callaway RM, Atwater DZ (2017) Ecotypic diversity of a dominant grassland species resists exotic invasion. Biol Invasions 19:1483–1493. https://doi.org/10.1007/s10530-017-1373-9
Yoder JB, Stanton-Geddes J, Zhou P, Briskine R, Young ND, Tiffin P (2014) Genomic signature of adaptation to climate in Medicago truncatula. Genetics 196:1263. https://doi.org/10.1534/genetics.113.159319
Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326–3328. https://doi.org/10.1093/bioinformatics/bts606
Zheng X, Gogarten SM (2015) SeqArray: Big data management of genome-wide sequence variants. R package version 1.10.6.https://github.com/zhengxwen/SeqArray. Accessed 1 Nov 2017
Acknowledgements
This work was supported by the U. S. National Science Foundation EAGER 1748133, DEB 1456955, DEB 1257965, and EF-01137363; and in part by an Institutional Development Award (IDeA) from the National Institute of General Medical Sciences of the National Institutes of Health under Grant number P20GM103451. This research was also supported by U. S. National Science Foundation grants to the University of New Mexico for Long-term Ecological Research. Thanks for field assistance from Anny Chung, Aaron Robinson, and Eva Dettweiler-Robinson.
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KDW and JAR conceived the genetic diversity study; SLC and WTP designed and established the EDGE drought experiment; JAR, DON and JB conducted field sampling; JB extracted the DNA; JM and AS performed the genotyping; JM, JAR, DON and KDW analyzed the data; KDW, JM, DON, SLC and JAR wrote the manuscript; KDW, JM, JAR, SLC, and WTP contributed funding for the study.
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Whitney, K.D., Mudge, J., Natvig, D.O. et al. Experimental drought reduces genetic diversity in the grassland foundation species Bouteloua eriopoda. Oecologia 189, 1107–1120 (2019). https://doi.org/10.1007/s00442-019-04371-7
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DOI: https://doi.org/10.1007/s00442-019-04371-7