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Genetic Covariation Between the Vertically Transmitted Endophyte Epichloë canadensis and Its Host Canada Wildrye

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Abstract

Symbiotic mutualisms are thought to be stabilized by correlations between the interacting genotypes which may be strengthened via vertical transmission and/or reduced genetic variability within each species. Vertical transmission, however, may weaken interactions over time as the endosymbionts would acquire mutations that could not be purged. Additionally, temporal variation in a conditional mutualism could create genetic variation and increased variation in the interaction outcome. In this study, we assessed genetic variation in both members of a symbiosis, the endosymbiotic fungal endophyte Epichloë canadensis and its grass host Canada wildrye (Elymus canadensis). Both species exhibited comparable levels of diversity, mostly within populations rather than between. There were significant differences between populations, although not in the same pattern for the two species, and the differences were not correlated with geographic distance for either species. Interindividual genetic distance matrices for the two species were significantly correlated, although all combinations of discriminant analysis of principle components (DAPC) defined multilocus genotype groups were found suggesting that strict genotype matching is not necessary. Variation in interaction outcome is common in grass/endophyte interactions, and our results suggest that the accumulation of mutations overtime combined with temporal variation in selection pressures increasing genetic variation in the symbiosis may be the cause.

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Data Availability

The data sets generated during the current study are available from the corresponding author on reasonable request.

References

  1. Bronstein JL (2015) The study of mutualism. In: Bronstein JL (ed) Mutualism. OUP Oxford, Oxford, United Kingdom

    Chapter  Google Scholar 

  2. Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592. https://doi.org/10.1016/j.tree.2006.06.018

    Article  PubMed  Google Scholar 

  3. Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53. https://doi.org/10.1016/S0169-5347(98)01529-8

    Article  CAS  PubMed  Google Scholar 

  4. Stoy KS, Gibson AK, Gerardo NM, Morran LT (2020) A need to consider the evolutionary genetics of host–symbiont mutualisms. J Evol Biol 33:1656–1668. https://doi.org/10.1111/jeb.13715

    Article  PubMed  Google Scholar 

  5. Wade MJ, Goodnight CJ (2006) Cyto-nuclear epistasis: two-locus random genetic drift in hermaphroditic and dioecious species. Evolution 60:643–659. https://doi.org/10.1111/j.0014-3820.2006.tb01146.x

    Article  CAS  PubMed  Google Scholar 

  6. Ewald P (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503:295–306. https://doi.org/10.1111/j.1749-6632.1987.tb40616.x

    Article  CAS  PubMed  Google Scholar 

  7. Frank SA (1994) Genetics of mutualism: the evolution of altruism between species. J Theor Biol 170:393–400. https://doi.org/10.1006/jtbi.1994.1200

    Article  CAS  PubMed  Google Scholar 

  8. Bennett GM, Moran NA (2015) Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. PNAS 112:10169–10176. https://doi.org/10.1073/pnas.1421388112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Herbeck JT, Funk DJ, Degnan PH, Wernegreen JJ (2003) A conservative test of genetic drift in the endosymbiotic bacterium Buchnera: slightly deleterious mutations in the chaperonin groEL. Genetics 165:1651–1660. https://doi.org/10.1093/genetics/165.4.1651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Moran NA (1996) Accelerated evolution and Muller’s rachet in endosymbiotic bacteria. Proc Natl Acad Sci 93:2873–2878. https://doi.org/10.1073/pnas.93.7.2873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. O’Fallon B (2008) Population structure, levels of selection, and the evolution of intracellular symbionts. Evolution 62:361–373. https://doi.org/10.1111/j.1558-5646.2007.00289.x

    Article  PubMed  Google Scholar 

  12. Chong RA, Moran NA (2016) Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts. PNAS 113:13114–13119. https://doi.org/10.1073/pnas.1610749113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Russell SL, Pepper-Tunick E, Svedberg J et al (2020) Horizontal transmission and recombination maintain forever young bacterial symbiont genomes. PLoS Genet 16:e1008935. https://doi.org/10.1371/journal.pgen.1008935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Brandvain Y, Goodnight C, Wade MJ (2011) Horizontal transmission rapidly erodes disequilibria between organelle and symbiont genomes. Genetics 189:397–404. https://doi.org/10.1534/genetics.111.130906

    Article  PubMed  PubMed Central  Google Scholar 

  15. Foster KR, Wenseleers T (2006) A general model for the evolution of mutualisms. J Evol Biol 19:1283–1293. https://doi.org/10.1111/j.1420-9101.2005.01073.x

    Article  CAS  PubMed  Google Scholar 

  16. Parker MA (1999) Mutualism in metapopulations of legumes and rhizobia. Am Nat 153:S48–S60. https://doi.org/10.1086/303211

    Article  PubMed  Google Scholar 

  17. Yoder JB, Nuismer SL, III AEEDB, Bronstein EJL (2010) When does coevolution promote diversification? Am Nat 176:802–817. https://doi.org/10.1086/657048

  18. Gomulkiewicz R, Nuismer SL, Thompson JN (2003) Coevolution in variable mutualisms. Am Nat 162:S80–S93. https://doi.org/10.1086/378705

    Article  PubMed  Google Scholar 

  19. Nuismer SL, Gomulkiewicz R, Morgan MT, Gavrilets AES (2003) Coevolution in temporally variable environments. Am Nat 162:195–204. https://doi.org/10.1086/376582

    Article  PubMed  Google Scholar 

  20. Nuismer SL, Thompson JN, Gomulkiewicz R (1999) Gene flow and geographically structured coevolution. Proc R Soc Lond Ser B Biol Sci 266:605–609. https://doi.org/10.1098/rspb.1999.0679

    Article  Google Scholar 

  21. Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:S1–S14. https://doi.org/10.1086/303208

    Article  Google Scholar 

  22. Thompson JN (1999) The evolution of species interactions. Science 284:2116–2118. https://doi.org/10.1126/science.284.5423.2116

    Article  CAS  PubMed  Google Scholar 

  23. Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297. https://doi.org/10.1146/annurev.es.21.110190.001423

    Article  Google Scholar 

  24. Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127. https://doi.org/10.1086/342161

    Article  PubMed  Google Scholar 

  25. Newman JA, Gillis S, Hager HA (2022) Costs, benefits, parasites and mutualists: the use and abuse of the mutualism–parasitism continuum concept for “Epichloë” fungi. Philos Theor Pract Biol 14:1–41. https://doi.org/10.3998/ptpbio.2103

  26. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. Trends Plant Sci 9:275–280. https://doi.org/10.1016/j.tplants.2004.04.005

    Article  CAS  PubMed  Google Scholar 

  27. Brem D, Leuchtmann A (2001) Epichloë grass endophytes increase herbivore resistance in the woodland grass Brachypodium sylvaticum. Oecologia 126:522–530. https://doi.org/10.1007/s004420000551

    Article  CAS  PubMed  Google Scholar 

  28. Decunta FA, Pérez LI, Malinowski DP et al (2021) A systematic review on the effects of Epichloë fungal endophytes on drought tolerance in cool-season grasses. Front Plant Sci 12:1–9. https://doi.org/10.3389/fpls.2021.644731

  29. 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

    Article  CAS  PubMed  Google Scholar 

  30. Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host–parasite interaction webs. Nature 409:78–81. https://doi.org/10.1038/35051070

    Article  CAS  PubMed  Google Scholar 

  31. Rudgers JA, Clay K (2008) An invasive plant–fungal mutualism reduces arthropod diversity. Ecol Lett 11:831–840. https://doi.org/10.1111/j.1461-0248.2008.01201.x

    Article  PubMed  Google Scholar 

  32. Saari S, Sundell J, Huitu O et al (2010) Fungal-mediated multitrophic interactions - do grass endophytes in diet protect voles from predators? PLoS One 5:e9845. https://doi.org/10.1371/journal.pone.0009845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ahlholm JU, Helander M, Lehtimäki S et al (2002) Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos 99:173–183. https://doi.org/10.1034/j.1600-0706.2002.990118.x

    Article  Google Scholar 

  34. Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. Am Nat 161:310–325. https://doi.org/10.1086/345937

    Article  PubMed  Google Scholar 

  35. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343. https://doi.org/10.2307/221711

    Article  Google Scholar 

  36. Saikkonen K, Wäli PR, Helander M (2010) Genetic compatibility determines endophyte-grass combinations. PLoS One 5:e11395. https://doi.org/10.1371/journal.pone.0011395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428–433. https://doi.org/10.1016/j.tplants.2006.07.001

    Article  CAS  PubMed  Google Scholar 

  38. Donald ML, Bohner TF, Kolis KM, Shadow RA, Rudgers JA, Miller TEX (2021) Context-dependent variability in the population prevalence and individual fitness effects of plant–fungal symbiosis. J Ecol 109:847–859. https://doi.org/10.1111/1365-2745.13510

    Article  CAS  Google Scholar 

  39. Popay AJ, Cox NR, Popay AJ, Cox NR (2021) Costs and benefits of hosting Epichloë endophytes: a comparison of three haplotypes in Lolium perenne with contrasting effects on two herbivores. Grass Research 1:1–10 https://doi.org/10.48130/GR-2021-0008

    Article  Google Scholar 

  40. Sullivan TJ, Rodstrom J, Vandop J, Librizzi J, Graham C, Schardl CL, Bultman TL (2007) Symbiont-mediated changes in Lolium arundinaceum inducible defenses: evidence from changes in gene expression and leaf composition. New Phytol 176:673–679. https://doi.org/10.1111/j.1469-8137.2007.02201.x

    Article  CAS  PubMed  Google Scholar 

  41. Cheplick GP (2008) Host genotype overrides fungal endophyte infection in influencing tiller and spike production of Lolium perenne (Poaceae) in a common garden experiment. Am J Bot 95:1063–1071. https://doi.org/10.3732/ajb.0800042

    Article  PubMed  Google Scholar 

  42. Cheplick GP, Cho R (2003) Interactive effects of fungal endophyte infection and host genotype on growth and storage in Lolium perenne. New Phytol 158:183–191. https://doi.org/10.1046/j.1469-8137.2003.00723.x

    Article  Google Scholar 

  43. Leuchtmann A, Schardl CL (2022) Genetic diversity of Epichloë endophytes associated with Brachypodium and Calamagrostis host grass genera including two new species. Journal of Fungi 8:1086. https://doi.org/10.3390/jof8101086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sneck ME, Rudgers JA, Young CA, Miller TEX (2017) Variation in the prevalence and transmission of heritable symbionts across host populations in heterogeneous environments. Microb Ecol 74:640–653. https://doi.org/10.1007/s00248-017-0964-4

    Article  PubMed  Google Scholar 

  45. Hitchcock AS (1971) Manual of the grasses of the United States, 2nd ed. (revised by A. Chase). Dover Publications, New York

    Google Scholar 

  46. Charlton ND, Craven KD, Mittal S, Hopkins AA, Young CA (2012) Epichloë canadensis, a new interspecific epichloid hybrid symbiotic with Canada wildrye (Elymus canadensis). Mycologia 104:1187–1199. https://doi.org/10.3852/11-403

    Article  PubMed  Google Scholar 

  47. Schardl CL, Leuchtmann A (1999) Three new species of Epichloë symbiotic with North American grasses. Mycologia 91:95–107. https://doi.org/10.1080/00275514.1999.12060996

    Article  Google Scholar 

  48. White JF, Bultman TL (1987) Endophyte-host associations in forage grasses. VIII. Heterothallism in Epichloë typhina. Am J Bot 74:1716. https://doi.org/10.2307/2444142

    Article  Google Scholar 

  49. Saha MC, Young CA, Hopkins AA (2009) Genetic variation within and among Wildrye (Elymus canadensis and E. virginicus) populations from the Southern Great Plains. Crop Sci 49:913–922. https://doi.org/10.2135/cropsci2008.04.0239

    Article  CAS  Google Scholar 

  50. Vogel KP, Hopkins AA, Moore KJ, Johnson KD, Carlson IT (2006) Genetic variation among Canada wildrye accessions from midwest USA remnant prairies for biomass yield and other traits. Crop Sci 46:2348. https://doi.org/10.2135/cropsci2006.01.0020

    Article  Google Scholar 

  51. Moon CD, Tapper BA, Scott B (1999) Identification of Epichloë endophytes in planta by a microsatellite-based PCR fingerprinting assay with automated analysis. Appl Environ Microbiol 65:1268–1279. https://doi.org/10.1128/AEM.65.3.1268-1279.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Moon CD, Scott B, Schardl CL, Christensen MJ (2000) The evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 92:1103–1118. https://doi.org/10.1080/00275514.2000.12061258

    Article  Google Scholar 

  53. Oberhofer M, Leuchtmann A (2014) Horizontal transmission, persistence and competition capabilities of Epichloë endophytes in Hordelymus europaeus grass hosts using dual endophyte inocula. Fungal Ecol 11:37–49. https://doi.org/10.1016/j.funeco.2014.04.005

    Article  Google Scholar 

  54. Sullivan TJ, Faeth SH (2004) Gene flow in the endophyte Neotyphodium and implications for coevolution with Festuca arizonica. Mol Ecol 13:649–656. https://doi.org/10.1046/j.1365-294X.2004.02091.x

    Article  CAS  PubMed  Google Scholar 

  55. Saha MC, Mian MAR, Eujayl I, Zwonitzer JC, Wang L, May GD (2004) Tall fescue EST-SSR markers with transferability across several grass species. Theor Appl Genet 109:783–791. https://doi.org/10.1007/s00122-004-1681-1

    Article  PubMed  Google Scholar 

  56. R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  57. Covarrubias-Pazaran G, Diaz-Garcia L, Schlautman B, Salazar W, Zalapa J (2016) Fragman: an R package for fragment analysis. BMC Genet 17:62. https://doi.org/10.1186/s12863-016-0365-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281. https://doi.org/10.7717/peerj.281

    Article  PubMed  PubMed Central  Google Scholar 

  59. McMillan E, Sun G (2004) Genetic relationships of tetraploid Elymus species and their genomic donor species inferred from polymerase chain reaction-restriction length polymorphism analysis of chloroplast gene regions. Theor Appl Genet 108:535–542. https://doi.org/10.1007/s00122-003-1453-3

    Article  CAS  PubMed  Google Scholar 

  60. Agapow P-M, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1:101–102. https://doi.org/10.1046/j.1471-8278.2000.00014.x

    Article  CAS  Google Scholar 

  61. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94

    Article  PubMed  PubMed Central  Google Scholar 

  62. Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Meirmans PG, Liu S, van Tienderen PH (2018) The analysis of polyploid genetic data. J Hered 109:283–296. https://doi.org/10.1093/jhered/esy006

    Article  CAS  PubMed  Google Scholar 

  64. Bruvo R, Michiels NK, D’souza TG, Schulenburg H (2004) A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol Ecol 13:2101–2106. https://doi.org/10.1111/j.1365-294X.2004.02209.x

    Article  CAS  PubMed  Google Scholar 

  65. Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20. https://doi.org/10.18637/jss.v022.i04

  66. Thioulouse J, Renaud S, Dufour A-B, Dray S (2021) Overcoming the spurious groups problem in between-group PCA. Evol Biol 48:458–471. https://doi.org/10.1007/s11692-021-09550-0

    Article  Google Scholar 

  67. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590. https://doi.org/10.1093/genetics/89.3.583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Dray S, Bauman D, Blanchet G, et al (2022) Adespatial: multivariate multiscale spatial analysis. R package version 0.3-16. https://CRAN.R-project.org/package=adespatial

  69. Dray S, Chessel D, Thioulouse J (2003) Co-inertia analysis and the linking of ecological data tables. Ecology 84:3078–3089. https://doi.org/10.1890/03-0178

    Article  Google Scholar 

  70. Oksanen J, Simpson GL, Blanchet FG, et al (2022) Vegan: community ecology package. R package version 2.6-4. https://CRAN.R-project.org/package=vegan

  71. Sneck ME, Rudgers JA, Young CA, Tex M (2019) Does host outcrossing disrupt compatibility with heritable symbionts? Oikos 128:892–903. https://doi.org/10.1111/oik.06182

    Article  Google Scholar 

  72. Meseguer AS, Manzano-Marín A, d'Acier AC, Clamens A-L, Godefroid M, Jousselin E (2017) Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts. Mol Ecol 26:2363–2378. https://doi.org/10.1111/mec.13910

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank Mark McKone and Nancy Barker for access to the Carleton College Cowling Arboretum, and the Iowa Department of Natural Resources for access to Hayden Prairie. The authors also thank two anonymous reviewers for their helpful feedback on the manuscript.

Funding

This research was supported by NSF-IOS-1119775 to TJS and TLB.

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TJS and TB conceived and designed the study. TJS, HR, and TB contributed to data collection. TJS preformed the analysis and wrote the initial draft, and all authors contributed to the editing. All the authors read and approved the final manuscript.

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Correspondence to T. J. Sullivan.

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Supplementary Information

Supplemental Fig. 1

Panels a (E. canadensis) and b (CWR) are minimum spanning networks for MLGs based on Bruvo’s distances. Node size is proportional to the number of MLGs, and nodes with MLGs represented in more than 1 population are plotted as pie charts (PNG 504 kb)

High resolution image (TIFF 2883 kb)

(PNG 743 kb)

High resolution image (TIFF 2883 kb)

Supplemental Table 1

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Sullivan, T.J., Roberts, H. & Bultman, T.L. Genetic Covariation Between the Vertically Transmitted Endophyte Epichloë canadensis and Its Host Canada Wildrye. Microb Ecol 86, 1686–1695 (2023). https://doi.org/10.1007/s00248-022-02166-7

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