Negative correlation between ash dieback susceptibility and reproductive success: good news for European ash forests

  • Devrim Semizer-CumingEmail author
  • Reiner Finkeldey
  • Lene Rostgaard Nielsen
  • Erik Dahl Kjær
Research Paper


Key message

European ash ( Fraxinus excelsior L.) trees with low susceptibility to ash dieback have higher reproductive fitness compared to highly susceptible trees, although most pronounced for female success. Selection at generation turnover therefore supports the future recovery of ash forests.


The introduced invasive pathogen Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz, and Hosoya cause extensive damage on European ash (Fraxinus excelsior L.). Heritable variation in susceptibility to ash dieback has been observed among ash trees in natural and planted populations, but it is not clear how variation in susceptibility influences reproductive fitness.


We hypothesize that healthier male and female trees contribute more gametes to the following generation compared to unhealthy ones.


We tested the hypothesis by studying gender, seed production, and paternal success in a clonal field trial with 39 replicated clones. In the trial, the susceptibility level of each clone has been recorded in terms of percent crown damage since 2007. We used a linear regression model to explore the relationship between susceptibility and reproductive success (female and male).


The clones revealed a clear gender dimorphism with an approximate 2:2:1 male/female/hermaphrodite ratio. Females with low levels of crown damage produced substantially more seeds compared to highly damaged females. The male clone with the lowest level of susceptibility was the most effective pollen donor, but highly susceptible males also sired some offspring.


The results overall represent good news for the potential recovery of ash forests: selection against most susceptible genotypes at generation turnover is expected to facilitate building up disease resistance in ash populations.


Ash dieback Fraxinus excelsior Fitness Gender Gene pool Reproductive success 



We thank Lene Hasmark Andersen for the help with lab work and Lars Nørgaard Hansen and Lea Vig McKinney for help with fieldwork. We thank Oliver Gailing for his comments on an earlier version of the manuscript. We are grateful to the two anonymous reviewers and the editors, Erwin Dreyer and Benoit Marçais, for their comments and suggestions.


This study was supported by the European Commission under the FONASO Erasmus Mundus Joint Doctorate Program and Villum Foundation (Grant no. VKR023062).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aggarwal RK, Allainguillaume J, Bajay MM, Barthwal S, Bertolino P, Chauhan P, Consuegra S, Croxford A, Dalton DL, den Belder E, Díaz-Ferguson E, Douglas MR, Drees M, Elderson J, Esselink GD, Fernández-Manjarrés JF, Frascaria-Lacoste N, Gäbler-Schwarz S, Garcia de Leaniz C, Ginwal HS, Goodisman MA, Guo B, Hamilton MB, Hayes PK, Hong Y, Kajita T, Kalinowski ST, Keller L, Koop BF, Kotzé A, Lalremruata A, Leese F, Li C, Liew WY, Martinelli S, Matthews EA, Medlin LK, Messmer AM, Meyer EI, Monteiro M, Moyer GR, Nelson RJ, Nguyen TT, Omoto C, Ono J, Pavinato VA, Pearcy M, Pinheiro JB, Power LD, Rawat A, Reusch TB, Sanderson D, Sannier J, Sathe S, Sheridan CK, Smulders MJ, Sukganah A, Takayama K, Tamura M, Tateishi Y, Vanhaecke D, Vu NV, Wickneswari R, Williams AS, Wimp GM, Witte V, Zucchi MI (2011) Permanent genetic resources added to Molecular Ecology Resources Database 1 August 2010–30 September 2010. Mol Ecol Resour 11:219–222. CrossRefPubMedGoogle Scholar
  2. Altizer S, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol 18:589–596. CrossRefGoogle Scholar
  3. Antos JA, Allen GA (1999) Patterns of reproductive effort in male and female shrubs of Oemleria cerasiformis: a 6-year study. J Ecol 87(1):77–84. CrossRefGoogle Scholar
  4. Bacles CF, Burczyk J, Lowe AJ, Ennos RA (2005) Historical and contemporary mating patterns in remnant populations of the forest tree Fraxinus excelsior L. Evol 59(5):979–990. CrossRefGoogle Scholar
  5. Bacles CFE, Ennos RA (2008) Paternity analysis of pollen-mediated gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Hered 101(4):368–380CrossRefGoogle Scholar
  6. Bacles CF, Lowe AJ, Ennos RA (2006) Effective seed dispersal across a fragmented landscape. Sci 311(5761):628–628. CrossRefGoogle Scholar
  7. Bai X, Rivera-Vega L, Mamidala P, Bonello P, Herms DA, Mittapalli O (2011) Transcriptomic signatures of ash (Fraxinus spp.) phloem. PLoS One 6:e16368. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bakys R, Vasaitis R, Barklund P, Ihrmark K, Stenlid J (2009) Investigations concerning the role of Chalara fraxinea in declining Fraxinus excelsior. Plant Pathol 58(2):284–292. CrossRefGoogle Scholar
  9. Baral HO, Queloz V, Hosoya T (2014) Hymenoscyphus fraxineus, the correct scientific name for the fungus causing ash dieback in Europe. IMA Fungus 5(1):79–80CrossRefGoogle Scholar
  10. Cipollini ML, Whigham DF (1994) Sexual dimorphism and cost of reproduction in the dioecious shrub Lindera benzoin (Lauraceae). Am J Bot 81(1):65–75. CrossRefGoogle Scholar
  11. Cleary MR, Andersson PF, Broberg A, Elfstrand M, Daniel G, Stenlid J (2014) Genotypes of Fraxinus excelsior with different susceptibility to the ash dieback pathogen Hymenoscyphus pseudoalbidus and their response to the phytotoxin viridiol—a metabolomic and microscopic study. Phytochem 102:115–125. CrossRefGoogle Scholar
  12. Cleary M, Nguyen D, Marčiulynienė D, Berlin A, Vasaitis R, Stenlid J (2016) Friend or foe? Biological and ecological traits of the European ash dieback pathogen Hymenoscyphus fraxineus in its native environment. Sci Rep 6:21895. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Enderle R, Nakou A, Thomas K, Metzler B (2014) Susceptibility of autochthonous German Fraxinus excelsior clones to Hymenoscyphus pseudoalbidus is genetically determined. Ann For Sci 72:183–193. CrossRefGoogle Scholar
  14. Gerard PR, Fernandez-Manjarres JF, Frascaria-Lacoste N (2006) Temporal cline in a hybrid zone population between Fraxinus excelsior L. and Fraxinus angustifolia Vahl: structure of an ash hybrid zone population. Mol Ecol 15:3655–3667. CrossRefPubMedGoogle Scholar
  15. Harper AL, McKinney LV, Nielsen LR, Havlickova L, Li Y, Trick M, Fraser F, Wang L, Fellgett A, Sollars ESA, Janacek SH, Downie JA, Buggs RJA, Kjær ED, Bancroft I (2016) Molecular markers for tolerance of European ash (Fraxinus excelsior) to dieback disease identified using associative transcriptomics. Sci Rep 6:19335. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program Cervus accommodates genotyping error increases success in paternity assignment: Cervus likelihood model. Mol Ecol 16:1099–1106. CrossRefPubMedGoogle Scholar
  17. Kjaer ED, McKinney LV, Nielsen LR, Hansen LN, Hansen JK (2012) Adaptive potential of ash (Fraxinus excelsior) populations against the novel emerging pathogen Hymenoscyphus pseudoalbidus: adaptive potential of F. excelsior. Evol Appl 5:219–228. CrossRefPubMedGoogle Scholar
  18. Korpelainen H (1992) Patterns of resource allocation in male and female plants of Rumex acetosa and R. acetosella. Oecologia 89(1):133–139CrossRefGoogle Scholar
  19. Lefort F, Brachet S, Frascaria-Lacoste N, Edwards KJ, Douglas GC (1999) Identification and characterization of microsatellite loci in ash (Fraxinus excelsior L.) and their conservation in the olive family (Oleaceae). Mol Ecol 8(6):1088–1089. CrossRefGoogle Scholar
  20. Lenz H, Bartha B, Straßer L, Lemme H (2016) Development of ash dieback in south-eastern Germany and the increasing occurrence of secondary pathogens. Forests 7:41. CrossRefGoogle Scholar
  21. Lobo A, Hansen JK, McKinney LV, Nielsen LR, Kjær ED (2014) Genetic variation in dieback resistance: growth and survival of Fraxinus excelsior under the influence of Hymenoscyphus pseudoalbidus. Scand J For Res 29(6):519–526. CrossRefGoogle Scholar
  22. Lobo A, McKinney LV, Hansen JK, Kjær ED, Nielsen LR (2015) Genetic variation in dieback resistance in Fraxinus excelsior confirmed by progeny inoculation assay. For Path 45:379–387. CrossRefGoogle Scholar
  23. Lygis V, Bakys R, Gustiene A, Burokiene D, Matelis A, Vasaitis R (2014) Forest self-regeneration following clear-felling of dieback-affected Fraxinus excelsior: focus on ash. Eur J For Res 133(3):501–510. CrossRefGoogle Scholar
  24. Marçais B, Husson C, Cael O, Dowkiw A, Saintonge F- X, Delahaye L, Collet C, Chanderlier A (2017) Estimation of ash mortality induced by Hymenoscyphus fraxineus in France and Belgium. Baltic For 23(1):159–167Google Scholar
  25. Marshall TC, Slate JB, Kruuk LE, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7(5):639–655. CrossRefPubMedGoogle Scholar
  26. Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinform 25:1982–1983. CrossRefGoogle Scholar
  27. McKinney LV, Nielsen LR, Hansen JK, Kjær ED (2011) Presence of natural genetic resistance in Fraxinus excelsior (Oleraceae) to Chalara fraxinea (Ascomycota): an emerging infectious disease. Hered 106:788–797CrossRefGoogle Scholar
  28. McKinney LV, Nielsen LR, Collinge DB, Thomsen IM, Hansen JK, Kjær ED (2014) The ash dieback crisis: genetic variation in resistance can prove a long-term solution. Plant Pathol 63(3):1–15. CrossRefGoogle Scholar
  29. Muñoz F, Marçais B, Dufour J, Dowkiw A (2016) Rising out of the ashes: additive genetic variation for crown and collar resistance to Hymenoscyphus fraxineus in Fraxinus excelsior. Phytopathol 106(12):1535–1543. CrossRefGoogle Scholar
  30. Nielsen LR, McKinney LV, Hietala AM, Kjær ED (2017) The susceptibility of Asian, European and North American Fraxinus species to the ash dieback pathogen Hymenoscyphus fraxineus reflects their phylogenetic history. Eur J For Res 136(1):59–73. CrossRefGoogle Scholar
  31. Noakes AG, Best T, Staton ME, Koch J, Romero-Severson J (2014) Cross amplification of 15 EST-SSR markers in the genus Fraxinus. Conserv Genet Resour 6(4):969–970. CrossRefGoogle Scholar
  32. Obeso JR (2002) The costs of reproduction in plants. New Phytol 155(3):321–348. CrossRefGoogle Scholar
  33. Pliûra A, Heuertz M (2003) EUFORGEN technical guidelines for genetic conservation and use for common ash (Fraxinus excelsior). International Plant Genetic Resources Institute, Rome, p 6Google Scholar
  34. Pliūra A, Lygis V, Suchockas V, Bartkevicius E (2011) Performance of twenty four European Fraxinus excelsior populations in three Lithuanian progeny trials with a special emphasis on resistance to Chalara fraxinea. Baltic For 17(1):17–34Google Scholar
  35. Primack RB, Kang H (1989) Measuring fitness and natural selection in wild plant populations. Annu Rev Ecol Syst 20:367–396. CrossRefGoogle Scholar
  36. Przybył K (2002) Fungi associated with necrotic apical parts of Fraxinus excelsior shoots. For Pathol 32:387–394. CrossRefGoogle Scholar
  37. Queenborough SA, Burslem DF, Garwood NC, Valencia R (2007) Determinants of biased sex ratios and inter-sex costs of reproduction in dioecious tropical forest trees. Am J Bot 94(1):67–78. CrossRefPubMedGoogle Scholar
  38. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Accessed 14 Jan 2019
  39. Santini A, Ghelardini L, De Pace C, Desprez-Loustau ML, Capretti P, Chandelier A, Cech T, Chira D, Diamandis S, Gaitniekis T, Hantula J (2013) Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol 197:238–250. CrossRefPubMedGoogle Scholar
  40. Semizer-Cuming D, Kjӕr ED, Finkeldey R (2017) Gene flow of common ash (Fraxinus excelsior L.) in a fragmented landscape. PLoS One 12(10):e0186757. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Skovsgaard JP, Thomsen IM, Skovgaard IM, Martinussen T (2010) Associations among symptoms of dieback in even-aged stands of ash (Fraxinus excelsior L.). For Pathol 40:7–18. CrossRefGoogle Scholar
  42. Sønstebø JH, Vivian-Smith A, Adamson K, Drenkhan R, Solheim H, Hietala A (2017) Genome-wide population diversity in Hymenoscyphus fraxineus points to an eastern Russian origin of European ash dieback. BioRxiv: 154492.
  43. Stener L-G (2013) Clonal differences in susceptibility to the dieback of Fraxinus excelsior in southern Sweden. Scand J For Resour 28:205–216. CrossRefGoogle Scholar
  44. Ueno N, Kanno H, Seiwa S (2006) Sexual differences in shoot production and leaf dynamics in a dioecious tree, Salix sachalinensis. Can J Bot 84:1852–1859. CrossRefGoogle Scholar
  45. Ueno N, Suyama Y, Seiwa K (2007) What makes the sex ratio female-biased in the dioecious tree Salix sachalinensis? J Ecol 95(5):951–959. CrossRefGoogle Scholar
  46. Wada KC, Takeno K (2010) Stress-induced flowering. Plant Signal Behav 5(8):944–947. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wallace CS, Rundel PW (1979) Sexual dimorphism and resource allocation in male and female shrubs of Simmondsia chinensis. Oecologia 44(1):34–39CrossRefGoogle Scholar
  48. Wickham H (2017) Tidyverse: easily install and load ‘Tidyverse’ packages. R package version 1.1.1.

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Forest Genetics and Forest Tree Breeding, Faculty of Forest Sciences and Forest EcologyGeorg-August University of GöttingenGöttingenGermany
  2. 2.Department of Geosciences and Natural Resource ManagementUniversity of CopenhagenFrederiksberg CDenmark
  3. 3.University of KasselKasselGermany

Personalised recommendations