Abstract
Mutualism between plants and arbuscular mycorrhizal (AM) fungi is common, and plant populations are expected to have adapted to the AM fungal communities occupying their roots. Tests of this hypothesis have frequently been done with plant populations that are tens to hundreds of kilometers apart. However, because AM fungal community composition differs at scales < 1 km, local adaptation of plant populations to AM fungi may occur at small spatial scales, but this prediction has not been tested. Furthermore, prior experiments do not often experimentally identify whether adaptation is related to specific mycorrhizal functions. To test for plant adaptation to AM fungal communities at small spatial scales, and whether adaptation is associated with the nutritional benefits that AM fungi provide to plants, we grew Lobelia siphilitica plants from two geographically close populations (1.4 km apart) in a greenhouse reciprocal transplant experiment with soil biota that either included (whole soil) or excluded AM fungi (microbial wash) at both low and high soil phosphorus availability. Though both plant populations responded positively to the presence of AM fungi in the whole soil biota treatment relative to the microbial wash treatment, the average growth response of plant populations to mycorrhizal fungi was highest when local populations were grown with local AM fungi. In addition, local adaptation was only observed in the presence of AM fungi at low phosphorus levels. Thus, local adaptation of plant populations to AM fungi is present at spatial scales that are much smaller than previously demonstrated and occurred primarily to enhance phosphorus acquisition.
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References
Ames RN, Mihara KL, Bethlenalvay GJ (1987) The establishment of microorganisms in vesicular-arbuscular mycorrhizal and control treatments. Biol Fertil Soils 3:217–223. https://doi.org/10.1007/BF00640633
Anacker BL, Klironomos JN, Maherali H, Reinhart KO, Strauss SY (2014) Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance. Ecol Lett 17:1613–1621. https://doi.org/10.1111/ele.12378
Baskett CA, Schemske DW (2015) Evolution and genetics of mutualism. In: Bronstein JL (ed) mutualism. Oxford University Press, Oxford, pp 77–92
Bever J (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977. https://doi.org/10.2307/1941601
Bronstein JL (2015) The study of mutualism. In: Bronstein JL (ed) mutualism. Oxford University Press, Oxford, pp 3–19
Brundrett MC (1994) Clearing and staining mycorrhizal roots. In: Brundrett MC, Melville L, Peterson L (eds) Practical methods in mycorrhizal research. Mycologue, Sidney, British Columbia, Canada, pp 42–46
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77. https://doi.org/10.1007/s11104-008-9877-9
Bucharova A (2017) Assisted migration within species range ignores biotic interactions and lacks evidence. Restoration Ecol 25:14–18. https://doi.org/10.1111/rec.12457
Bucharova A, Bossdorf O, Hölzel N, Kollmann J, Prasse R, Durka W (2018) Mix and match: regional admixture provenancing strikes a balance among different seed-sourcing strategies for ecological restoration. Conserv Genet 20:7–17. https://doi.org/10.1007/s10592-018-1067-6
Cahill JF Jr, Cale JA, Karst J, Bao T, Pec GJ, Erbilgin N (2017) No silver bullet: different soil handling techniques are useful for different research questions, exhibit differential type I and II error rates, and are sensitive to sampling intensity. New Phytol 216:11–14. https://doi.org/10.1111/nph.14141
Caruso CM (2012) Sexual dimorphism in floral traits of gynodioecious Lobelia siphilitica (Lobeliaceae) is consistent across populations. Botany 90:1245–1251. https://doi.org/10.1139/b2012-094
Caruso CM, Peterson SB, Ridley CE (2003) Natural selection on floral traits of Lobelia (Lobeliaceae): spatial and temporal variation. Am J Bot 90:1333–1340. https://doi.org/10.3732/ajb.90.9.1333
Caruso CM, Maherali H, Sherrard M (2006) Plasticity of physiology in Lobelia: testing for adaptation and constraint. Evolution 60:980–990. https://doi.org/10.1554/06-050.1
Caruso CM, Benscoter AM, Gale NV, Seifert EK, Mills ER, Case AL (2015) Effects of crossing distance on performance of the native wildflower Lobelia siphilitica: implications for ecological restoration. J Torrey Bot Soc 142:140–151. https://doi.org/10.3159/TORREY-D-13-00055.1
Clausen J, Keck DD, Hiesey WM (1948) Experimental studies on the nature of species. III. Environmental responses of climactic races of Achillea, 581st edn. Carnegie Institute of Washington Publication, Washington, p 129
Daniels BA, McCool PM, Menge JA (1981) Comparative inoculum potential of spores of six vesicular-arbuscular mycorrhizal fungi. New Phytol 89:385–391. https://doi.org/10.1111/j.1469-8137.1981.tb02319.x
Darwin CR (1862) On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing. John Murray, London
Davison J, Öpik M, Zobel M, Vasar M, Metsis M, Moora M (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS One 7:e41938. https://doi.org/10.1371/journal.pone.0041938
Delavaux CS, Smith-Ramesh LM, Kuebbing SE (2017) Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98:2111–2119. https://doi.org/10.1002/ecy.1892
Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233. https://doi.org/10.1146/annurev.es.19.110188.001231
Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443. https://doi.org/10.1111/j.1365-2435.2006.01228.x
Hagen M, Wikelski M, Kissling WD (2011) Space use of bumblebees (Bombus spp.) revealed by radio-tracking. PloS One 6:e19997. https://doi.org/10.1371/journal.pone.0019997
Harder LD, Johnson SD (2009) Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol 183:530–545. https://doi.org/10.1111/j.1469-8137.2009.02914.x
Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588. https://doi.org/10.1086/597611
Hoeksema JD, Forde SE (2008) A meta-analysis of factors affecting local adaptation between interacting species. Am Nat 171:275–290. https://doi.org/10.1086/527496
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GW, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x
Hovatter SR, Dejelo C, Case AL, Blackwood CB (2011) Metacommunity organization of soil microorganisms depends on habitat defined by presence of Lobelia siphilitica plants. Ecology 92:57–65. https://doi.org/10.1890/10-0332.1
Hovatter SR, Blackwood CB, Case AL (2013) Conspecific plant-soil feedback scales with population size in Lobelia siphilitica (Lobeliaceae). Oecologia 173:1295–1307. https://doi.org/10.1007/s00442-013-2710-z
Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647. https://doi.org/10.1111/j.1469-8137.2009.03110.x
Johnson NC, Wilson GW, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci USA 107:2093–2098. https://doi.org/10.1073/pnas.0906710107
Johnston MO (1991) Natural selection on floral traits in two species of Lobelia with different pollinators. Evolution 45:1468–1479. https://doi.org/10.2307/2409893
Kahiluoto H, Ketoja E, Vestberg M, Saarela I (2001) Promotion of AM utilization through reduced P fertilization 2. Field studies. Plant Soil 231:65–79. https://doi.org/10.1023/A:1010366400009
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x
Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR (2004) High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proc Natl Acad Sci USA 101:2369–2374. https://doi.org/10.1073/pnas.0306441101
Koide RT, Li M (1989) Appropriate controls for vesicular-arbuscular mycorrhiza research. New Phytol 111:35–44. https://doi.org/10.1111/j.1469-8137.1989.tb04215.x
Koske RE, Tessier B (1983) A convenient, permanent slide mounting medium. Newsl Mycol Soc Am 34:59
Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS One 3:e4010. https://doi.org/10.1371/journal.pone.0004010
Lin G, McCormack ML, Guo D (2015) Arbuscular mycorrhizal fungal effects on plant competition and community structure. J Ecol 103:1224–1232. https://doi.org/10.1111/1365-2745.12429
Maherali H, Oberle B, Stevens PF, Cornwell WK, McGlinn DJ (2016) Mutualism persistence and abandonment during the evolution of the mycorrhizal symbiosis. Am Nat 188:E113–E125. https://doi.org/10.1086/688675
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:68–73. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411. https://doi.org/10.1016/S0169-5347(00)89157-0
Pánková H, Münzbergová Z, Rydlová J, Vosátka M (2014a) Co-adaptation of plants and communities of arbuscular mycorrhizal fungi to their soil conditions. Folia Geobot 49:521–540. https://doi.org/10.1007/s12224-013-9183-z
Pánková H, Raabová J, Münzbergová Z (2014b) Mycorrhizal symbiosis and local adaptation in Aster amellus: a field transplant experiment. PLoS One 9:e93967. https://doi.org/10.1371/journal.pone.0093967
Pregitzer CC, Bailey JK, Hart SC, Schweitzer JA (2010) Soils as agents of selection: feedbacks between plants and soils alter seedling survival and performance. Evol Ecol 24:1045–1059. https://doi.org/10.1007/s10682-010-9363-8
Raabová J, Münzbergová Z, Fischer M (2011) The role of spatial scale and soil for local adaptation in Inula hirta. Basic Appl Ecol 12:152–160. https://doi.org/10.1016/j.baae.2011.01.001
Ravnskov S, Jakobsen I (1995) Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol 129:611–618. https://doi.org/10.1111/j.1469-8137.1995.tb03029.x
Reinhart KO, Rinella MJ (2016) A common soil handling technique can generate incorrect estimates of soil biota effects on plants. New Phytol 210:786–789. https://doi.org/10.1111/nph.13822
Rúa MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C, Lamit LJ, Piculell BJ, Bever JD, Zabinski C, Meadow JF, Lajeunesse MJ, Milligan BG, Karst J, Hoeksema JD (2016) Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:122. https://doi.org/10.1186/s12862-016-0698-9
Schreiner RP, Scagel CF (2016) Arbuscule frequency in grapevine roots is more responsive to reduction in photosynthetic capacity than to increased levels of shoot phosphorus. J Am Soc Hort Sci 141:151–161
Schultz PA, Miller MR, Jastrow JD, Rivetta CV, Bever JD (2001) Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies. Am J Bot 88:1650–1656. https://doi.org/10.2307/3558410
Schweiger PF, Robson AD, Barrow NJ (1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytol 131:247–254
Sherrard ME, Maherali H (2012) Local adaptation across a fertility gradient is influenced by soil biota in the invasive grass, Bromus inermis. Evol Ecol 26:529–544. https://doi.org/10.1007/s10682-011-9518-2
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792. https://doi.org/10.1126/science.3576198
Smith S, Read D (2008) Mycorrhizal Symbiosis, 3rd edn. Elsevier, Berlin
Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524. https://doi.org/10.1111/j.1469-8137.2004.01039.x
Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman and Co., New York
Stanescu S, Maherali H (2017) Arbuscular mycorrhizal fungi alter the competitive hierarchy among old-field plant species. Oecologia 183:479–491. https://doi.org/10.1007/s00442-016-3771-6
Umbanhowar J, McCann K (2005) Simple rules for the coexistence and competitive dominance of plants mediated by mycorrhizal fungi. Ecol Lett 8:247–252. https://doi.org/10.1111/j.1461-0248.2004.00714.x
Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Env Microb 64:5004–5007
Acknowledgements
We thank E. Bothwell and C.M. Caruso for assistance at various stages of the project, and the two anonymous reviewers for their thoughtful comments on the manuscript.
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This research was funded by a grant (RGPIN 261300-2013) from the Natural Sciences and Engineering Research Council of Canada (NSERC).
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PR and HM developed the hypotheses and designed the study. PR carried out the research. PR and HM analyzed data and co-wrote the manuscript.
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Communicated by Sarah M. Emery.
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Rekret, P., Maherali, H. Local adaptation to mycorrhizal fungi in geographically close Lobelia siphilitica populations. Oecologia 190, 127–138 (2019). https://doi.org/10.1007/s00442-019-04412-1
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DOI: https://doi.org/10.1007/s00442-019-04412-1