Abstract
Because genotypes within a species commonly differ in traits that influence other species, whole communities, or even ecosystem functions, evolutionary change within one key species may affect the community and ecosystem processes. Here we use experimental mesocosms to test how the evolution of reduced cooperation in rhizobium mutualists in response to 20 years of nitrogen fertilization compares to the effects of rhizobium presence on soil nitrogen availability and plant community composition and diversity. The evolution of reduced rhizobium cooperation caused reductions in soil nitrogen, biological nitrogen fixation, and leaf nitrogen concentrations that were as strong as, or even stronger than, experimental rhizobium inoculation (presence/absence) treatments. Effects of both rhizobium evolution and rhizobium inoculation on legume dominance, plant community composition, and plant species diversity were often smaller in magnitude, but suggest that rhizobium evolution can alter the relative abundance of plant functional groups. Our findings indicate that the consequences of rapid microbial evolution for ecosystems and communities can rival the effects resulting from the presence or abundance of keystone mutualists.
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Availability of data and material
Data used in this paper has been made publically available from the Dryad Data Repository (https://doi.org/10.5061/dryad.cfxpnvx6t). Rhizobium strains used in this experiment are available upon reasonable request from JAL or KDH.
Code availability
Code used for the data analyses presented in this paper has been made publically available from the Dryad Data Repository (https://doi.org/10.5061/dryad.cfxpnvx6t).
References
Akçay E, Simms EL (2011) Negotiation, sanctions, and context dependency in the legume-rhizobium mutualism. Am Nat 178:1–14. https://doi.org/10.1086/659997
Arrese-Igor C, Minchin FR, Gordon AJ, Nath AK (1997) Possible causes of the physiological decline in soybean nitrogen fixation in the presence of nitrate. J Exp Bot 48:905–913. https://doi.org/10.1093/jxb/48.4.905
Bassar RD, Marshall MC, López-Sepulcre A, Zandonà E, Auer SK, Travis J, Pringle CM, Flecker AS, Thomas SA, Fraser DF, Reznick DN (2010) Local adaptation in Trinidadian guppies alters ecosystem processes. Proc Nat Acad Sci 107:3616–3621. https://doi.org/10.1073/pnas.0908023107
Bauer JT, Kleczewski NM, Bever JD, Clay K, Reynolds HL (2012) Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities. Oecologia 170:1089–1098. https://doi.org/10.1007/s00442-012-2363-3
Becks L, Ellner SP, Jones LE, Hairston NG Jr (2012) The functional genomics of an eco-evolutionary feedback loop: linking gene expression, trait evolution, and community dynamics. Ecol Lett 15:492–501. https://doi.org/10.1111/j.1461-0248.2012.01763.x
Bradshaw WE, Holzapfel CM (2006) Evolutionary responses to rapid climate change. Science 312:1477–1478. https://doi.org/10.1126/science.1127000
Bronstein JL (2015) Mutualism. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:oso/9780199675654.001.0001
Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744. https://doi.org/10.1126/science.285.5434.1742
Declerck SAJ, Malo AR, Diehl S, Waasdorp D, Lemmen KD, Proios K, Papakostas S (2015) Rapid adaptation of herbivore consumers to nutrient limitation: eco-evolutionary feedbacks to population demography and resource control. Ecol Lett 18:553–562. https://doi.org/10.1111/ele.12436
Dickson TL, Gross KL (2013) Plant community responses to long-term fertilization: changes in functional group abundance drive changes in species richness. Oecologia 173:1513–1520. https://doi.org/10.1007/s00442-013-2722-8
Fitzpatrick CR, Agrawal AA, Basiliko N, Hastings AP, Isaac ME, Preston M, Johnson MTJ (2015) The importance of plant genotype and contemporary evolution for terrestrial ecosystem processes. Ecology 96:2632–2642. https://doi.org/10.1890/14-2333.1
Gomez P, Paterson S, De Meester L, Liu X, Lenzi L, Sharma MD, McElroy K, Buckling A (2016) Local adaptation of a bacterium is as important as its presence in structuring a natural microbial community. Nat Commun 7:12453. https://doi.org/10.1038/ncomms12453
Grman E, Robinson TMP, Klausmeier CA (2012) Ecological specialization and trade affect the outcome of negotiations in mutualism. Am Nat 179:567–581. https://doi.org/10.1086/665006
Hairston NG, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127. https://doi.org/10.1111/j.1461-0248.2005.00812.x
Haskett TL, Terpolilli JJ, Bekuma A, O’Hara GW, Sullivan JT, Wang P, Ronson CW, Ransay JP (2016) Assembly and transfer of tripartite integrative and conjugative genetic elements. Proc Natl Acad Sci USA 113:12268–12273. https://doi.org/10.1073/pnas.1613358113
Heath KD, Tiffin P (2007) Context dependence in the coevolution of plant and rhizobial mutualists. Proc R Soc B 274:1905–1912. https://doi.org/10.1098/rspb.2007.0495
Heath KD, Stock AJ, Stinchcombe JR (2010) Mutualism variation in the nodulation response to nitrate. J Evol Biol 23:2494–2500. https://doi.org/10.1111/j.1420-9101.2010.02092.x
Heath KD, Podowski JC, Heniff S, Klinger CR, Burke PV, Weese DJ, Yang WH, Lau JA (2020) Light availability and rhizobium variation interactively mediate the outcomes of legume-rhizobium symbiosis. Am J Bot 107:229–238. https://doi.org/10.1002/ajb2.1435
Hendry AP (2020) Eco-evolutionary dynamics. Princeton University Press, New Haven. https://doi.org/10.1515/9781400883080
Herman D, Brooks P, Ashraf M, Azam F, Mulvaney R (1995) Evaluation of methods for nitrogen-15 analysis of inorganic nitrogen in soil extracts. II diffusion methods. Commun Soil Sci Plant Anal 26:1675–1685. https://doi.org/10.1080/00103629509369400
Hoeksema JD, Schwartz MW (2003) Expanding comparative-advantage biological market models: contingency of mutualism on partner’s resource requirements and acquisition trade-offs. Proc R Soc B 270:913–919. https://doi.org/10.1098/rspb.2002.2312
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phyt 135:575–586. https://doi.org/10.1046/j.1469-8137.1997.00729.x
Kardol P, De Long JR, Mariotte P (2018) Soil biota as drivers of plant community assembly. In: Ohgushi T, Wurst S, Johnson A (eds) Aboveground–belowground community ecology. Ecological studies (analysis and synthesis), vol 234. Springer, Cham. https://doi.org/10.1007/978-3-319-91614-9_13
Keller KR (2014) Mutualistic rhizobia reduce plant diversity and alter community composition. Oecologia 176:1101–1109. https://doi.org/10.1007/s00442-014-3089-1
Keller KR, Lau JA (2018) When mutualisms matter: rhizobia effects on plant communities depend on host plant population and soil nitrogen availability. J Ecol 106:1046–1056. https://doi.org/10.1111/1365-2745.12938
Keller KR, Carabajal S, Navarro F, Lau JA (2018) Effects of multiple mutualists on plants and their associated arthropod communities. Oecologia 186:185–194. https://doi.org/10.1007/s00442-017-3984-3
Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474. https://doi.org/10.1111/j.1461-0248.2010.01538.x
Klinger CK, Lau JA, Heath KD (2016) Ecological genomics of mutualism decline in nitrogen-fixing bacteria. Proc R Soc B 283:20152563. https://doi.org/10.1098/rspb.2015.2563
Kohl DH, Shearer G, Harper JE (1980) Estimates of N2 fixation based on differences in the natural abundance of 15N in nodulating and nonnodulating isolines of soybeans. Plant Phys 66:61–65. https://doi.org/10.1104/pp.66.1.61
Lau JA (2006) Evolutionary responses of native plants to novel community members. Evolution 60:56–63. https://doi.org/10.1554/05-376.1
Lau JA, Suwa T (2016) The changing nature of plant-microbe interactions during a biological invasion. Biol Invasions 18:3527–3534. https://doi.org/10.1007/s10530-016-1245-8
Lau JA, terHorst CP (2019) Evolutionary responses to global change in species-rich communities. Ann New York Acad Sci. https://doi.org/10.1111/nyas.14221
Magnoli SM, Lau JA (2020) Evolution in novel environments: do restored prairie populations experience strong selection? Ecology 101:e03120. https://doi.org/10.1002/ecy.3120
Nguyen MA, Ortega AE, Nguyen KQ, Kimball S, Goulden ML, Funk JL (2016) Evolutionary responses of invasive grass species to variation in precipitation and soil nitrogen. J Ecol 104:979–986. https://doi.org/10.1111/1365-2745.12582
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) vegan: community ecology package. R Package version 2.0-10 http://cran.r-project.org/package=vegan
Palkovacs EP, Marshall MC, Lamphere BA, Lynch BR, Weese DJ, Fraser DF, Reznick DN, Pringle CM, Kinnison MT (2009) Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams. Phil Proc R Soc B 364:1617–1628. https://doi.org/10.1098/rstb.2009.0016
Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790. https://doi.org/10.1126/science.293.5536.1786
Porter SS, Sachs JL (2020) Agriculture and the disruption of plant-microbial symbiosis. Trends Ecol Evol 35:426–439. https://doi.org/10.1016/j.tree.2020.01.006
Ray JD, Sinclair TR (1998) The effect of pot size on growth and transpiration of maize and soybean during water deficit stress. J Exp Bot 49:1381–1386. https://doi.org/10.1093/jxb/49.325.1381
Regus JU, Wendlandt CE, Bantay RM, Gano-Cohen KA, Gleason NJ, Hollowell AC, O’Neill MR, Shahin KK, Sachs JL (2017) Nitrogen deposition decreases the benefits of symbiosis in a native legume. Plant Soil 414:159–170. https://doi.org/10.1007/s11104-016-3114-8
Schaum C-E, Barton S, Bestion E, Buckling A, Garcia-Carreras B, Lopez P, Lowe C, Pawar S, Smirnoff N, Trimmer M, Yvon-Durocher G (2017) Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nat Ecol Evol 1:0094. https://doi.org/10.1038/s41559-017-0094
Schlüter L, Lohbeck KT, Gutowska MA, Gröger JP, Riebesell U, Reusch TBH (2014) Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat Clim Change 4:1024–1030. https://doi.org/10.1038/nclimate2379
Schoener TW (2011) The newest synthesis: Understanding the interplay of evolutionary and ecological dynamics. Science 331:426–429. https://doi.org/10.1126/science.1193954
Schwartz MD, Hoeksema JD (1998) Specialization and resource trade: biological markets as a model of mutualisms. Ecology 79:1029–1038. https://doi.org/10.1890/0012-9658(1998)079[1029:SARTBM]2.0.CO;2
Simonsen AK, Han S, Rentschler CS, Heath KD, Stinchcombe JR (2015) Short-term fertilizer application alters phenotypic traits of symbiotic nitrogen fixing bacteria. PeerJ 8:e1291. https://doi.org/10.7717/peerj.1291
Six DL (2009) Climate change and mutualism. Nat Rev Microbiol 7:686. https://doi.org/10.1038/nrmicro2232
Snaydon RW, Davies TM (1982) Rapid divergence of plant populations in response to recent changes in soil conditions. Evolution 36:289–297. https://doi.org/10.1111/j.1558-5646.1982.tb05044.x
Strauss SY, Lau JA, Schoener TW, Tiffin P (2008) Evolution in ecological field experiments: implications for effect size. Ecol Lett 11:199–207. https://doi.org/10.1111/j.1461-0248.2007.01128.x
ter Horst CP, Zee PC (2016) Eco-evolutionary dynamics in plant-soil feedbacks. Funct Ecol 30:1062–1072. https://doi.org/10.1111/1365-2435.12671
ter Horst CP, Lennon JT, Lau JA (2014) The relative importance of rapid evolution for plant-soil feedbacks depends on ecological context. Proc R Soc B. https://doi.org/10.1098/rspb.2014.0028
Turley NE, Odell WC, Schaefer H, Everwand G, Crawley MJ, Johnson MTJ (2013) Contemporary evolution of plant growth rate following experimental removal of herbivores. Am Nat 181:S21–S34. https://doi.org/10.1086/668075
Unkovich MJ, Pate JS (1998) Symbiotic effectiveness and tolerance to early season nitrate in indigenous populations of subterranean clover rhizobia from S.W. Australian Pastures. Soil Biol Biochem 30:1435–1443. https://doi.org/10.1016/S0038-0717(97)00258-7
van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phyt 172:739–752. https://doi.org/10.1111/j.1469-8137.2006.01862.x
van Diepen LTA, Frey SD, Landis EA, Morrison EW, Pringle A (2017) Fungi exposed to chronic nitrogen enrichment are less able to decay leaf litter. Ecology 98:5–11. https://doi.org/10.1002/ecy.1635
Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawai’i: plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59:247–265. https://doi.org/10.2307/1942601
Weese DJ, Heath KD, Dentinger BTM, Lau JA (2015) Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution 69:631–642. https://doi.org/10.1111/evo.12594
Wendlandt CE, Gano-Cohen KA, Stokes PJN, Jonnala BNR, Zomorrodian AJ, Al-Moussawi K, Sachs JL (2022) Wild legumes maintain beneficial soil rhizobia populations despite decades of nitrogen deposition. Oecologia 198:419–430. https://doi.org/10.1007/s00442-022-05116-9
West SA, Kiers ET, Simms EL, Denison RF (2002) Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc R Soc B 269:685–694. https://doi.org/10.1098/rspb.2001.1878
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989. https://doi.org/10.1128/MMBR.63.4.968-989.1999
Acknowledgements
We thank Kane Keller for advice on constructing the experimental mesocosms, members of the Lau lab for help harvesting the experiment, and members of the Lau and Heath labs for comments on earlier versions of this manuscript. We appreciate help from Jonathan Treffkorn, Sheeri Hanjra, Lily Zhao, Adam Cullian, Nate Lawrence, Shuying Guo, and Zoe Frankowicz in processing and analyzing the leaf samples. This is KBS publication #2327.
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This research was supported by NSF DEB-1257756 awarded to JAL and KDH, by the NSF Long-Term Ecological Research Program at the Kellogg Biological Station (NSF DEB-1637653) and by Michigan State University AgBioResearch.
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JAL, KDH, and DJW conceived the experiments. JAL, DJW, and MDH designed the experiments. DSW, JES, and MDH performed the experiments. WHY conducted the isotope analyses. JAL and DJW analyzed the data. JAL and DJW wrote the bulk of the initial manuscript; WHY wrote the isotope analysis methods; all other authors edited the manuscript.
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Communicated by Joel Sachs.
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Lau, J.A., Hammond, M.D., Schmidt, J.E. et al. Contemporary evolution rivals the effects of rhizobium presence on community and ecosystem properties in experimental mesocosms. Oecologia 200, 133–143 (2022). https://doi.org/10.1007/s00442-022-05253-1
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DOI: https://doi.org/10.1007/s00442-022-05253-1