The Longevity of Colonies of Fungus-Growing Termites and the Stability of the Symbiosis.

Margo Wisselink, Duur K Aanen, Anouk van 't Padje
Author Information
  1. Margo Wisselink: Laboratory of Genetics, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.
  2. Duur K Aanen: Laboratory of Genetics, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.
  3. Anouk van 't Padje: Laboratory of Genetics, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands. ORCID

Abstract

The agricultural mutualistic symbiosis between macrotermitine termites and fungi is obligate for both partners. The termites provide a protective growth environment for the fungus by cultivating it inside their colony and providing it with foraged plant material. The termites use the fungus for plant substrate degradation, and the production of asexual fruiting bodies for nourishment and re-inoculation of the fungus garden. The termite colony can reach an age of up to several decades, during which time it is believed that a single fungal monoculture is asexually propagated by the offspring of a single founding royal pair. The termite-fungus mutualism has a long evolutionary history dating back more than 30 million years. Both on the time-scale of a termite colony lifespan and that of the mutualistic symbiosis, questions arise about stability. We address the physical stability of the mound, the termite colony and the monoculture fungal garden during a colony's lifetime. On the long-term evolutionary scale, we address the stability of the symbiosis, where horizontal transmission of the symbiotic fungus raises the question of how the mutualistic interaction between host and symbiont persists over generations.

Keywords

References

  1. BMC Evol Biol. 2019 Aug 23;19(1):172 [PMID: 31443631]
  2. Microb Ecol. 2012 May;63(4):975-85 [PMID: 22173371]
  3. Biotechnol Bioeng. 1974 Oct;16(10):1373-92 [PMID: 4429794]
  4. Nat Commun. 2013;4:1879 [PMID: 23695673]
  5. Mol Ecol. 2011 May;20(9):2023-33 [PMID: 21410808]
  6. Biol Lett. 2006 Jun 22;2(2):209-12 [PMID: 17148364]
  7. Curr Biol. 2019 Jun 3;29(11):R442-R447 [PMID: 31163154]
  8. PLoS One. 2013;8(2):e56464 [PMID: 23437139]
  9. Science. 2009 Mar 27;323(5922):1687 [PMID: 19325106]
  10. J Econ Entomol. 2015 Feb;108(1):266-73 [PMID: 26470129]
  11. Mol Ecol. 2002 Aug;11(8):1565-72 [PMID: 12144675]
  12. Biol Lett. 2020 Aug;16(8):20200394 [PMID: 32781906]
  13. Nat Rev Microbiol. 2010 Mar;8(3):218-30 [PMID: 20157340]
  14. J Chem Ecol. 2017 Oct;43(10):986-995 [PMID: 29124530]
  15. Proc Biol Sci. 2019 May 15;286(1902):20190128 [PMID: 31039713]
  16. Mol Ecol. 2009 Feb;18(3):553-67 [PMID: 19161474]
  17. Curr Biol. 2019 Aug 19;29(16):2758-2765.e6 [PMID: 31402298]
  18. Science. 2014 Nov 21;346(6212):922-3 [PMID: 25414293]
  19. Am Nat. 2011 Mar;177(3):288-300 [PMID: 21460538]
  20. Nutr Rev. 2012 Aug;70 Suppl 1:S2-9 [PMID: 22861804]
  21. Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14887-92 [PMID: 12386341]
  22. Nat Commun. 2016 May 03;7:11435 [PMID: 27139112]
  23. Ecology. 2006 Jul;87(7):1627-36 [PMID: 16922314]
  24. J Evol Biol. 2010 Dec;23(12):2507-28 [PMID: 20942825]
  25. Ecology. 2014 May;95(5):1384-93 [PMID: 25000769]
  26. Evolution. 2015 Apr;69(4):1091-9 [PMID: 25688421]
  27. Proc Biol Sci. 2017 Jul 26;284(1859): [PMID: 28747481]
  28. Proc Biol Sci. 2012 Sep 7;279(1742):3565-71 [PMID: 22719037]
  29. Mol Ecol. 2006 Oct;15(11):3131-8 [PMID: 16968259]
  30. Am Nat. 2014 Jun;183(6):762-70 [PMID: 24823820]
  31. Trends Ecol Evol. 2011 Apr;26(4):175-82 [PMID: 21296451]
  32. PeerJ. 2019 Jan 16;6:e6237 [PMID: 30671290]
  33. Ecol Lett. 2009 Jan;12(1):13-21 [PMID: 19019195]
  34. Genome Biol Evol. 2011;3:1107-18 [PMID: 21821597]
  35. Nature. 2000 Aug 17;406(6797):718-22 [PMID: 10963595]
  36. PLoS One. 2013 May 31;8(5):e65416 [PMID: 23741492]
  37. Proc Biol Sci. 1996 Mar 22;263(1368):339-44 [PMID: 8920255]
  38. Mycology. 2018 Jul 30;9(4):307-315 [PMID: 30533255]
  39. Mol Ecol. 2011 Jun;20(12):2619-27 [PMID: 21481052]
  40. BMC Evol Biol. 2007 Jul 13;7:115 [PMID: 17629911]
  41. Nat Commun. 2018 Jul 30;9(1):2970 [PMID: 30061657]
  42. BMC Evol Biol. 2014 Jun 05;14:121 [PMID: 24902958]
  43. Mycologia. 2014 Jul-Aug;106(4):642-8 [PMID: 24891414]
  44. Trends Genet. 2010 Aug;26(8):345-52 [PMID: 20594608]
  45. Curr Biol. 2006 Jul 11;16(13):R482-3 [PMID: 16824903]
  46. Nature. 2003 Sep 4;425(6953):78-81 [PMID: 12955144]
  47. Oecologia. 1991 May;86(3):424-432 [PMID: 28312932]
  48. PLoS One. 2016 Jun 22;11(6):e0156847 [PMID: 27333288]
  49. Science. 2011 Aug 12;333(6044):880-2 [PMID: 21836016]
  50. Mol Biol Evol. 2015 Oct;32(10):2775-83 [PMID: 26163667]
  51. Proc Biol Sci. 2018 Dec 19;285(1893):20182233 [PMID: 30963893]
  52. Environ Microbiol. 2015 Aug;17(8):2562-72 [PMID: 25581852]
  53. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5764-8 [PMID: 16592723]
  54. Science. 2009 Nov 20;326(5956):1103-6 [PMID: 19965427]
  55. Proc Biol Sci. 2010 Feb 7;277(1680):359-65 [PMID: 19828546]
  56. Mycol Res. 2005 Mar;109(Pt 3):314-8 [PMID: 15912948]

Grants

  1. 86514007/Nederlandse Organisatie voor Wetenschappelijk Onderzoek

Word Cloud

Created with Highcharts 10.0.0funguscolonymutualisticsymbiosistermitestermitestabilityplantgardensinglefungalmonoculturemutualismevolutionaryaddresshorizontaltransmissionagriculturalmacrotermitinefungiobligatepartnersprovideprotectivegrowthenvironmentcultivatinginsideprovidingforagedmaterialusesubstratedegradationproductionasexualfruitingbodiesnourishmentre-inoculationcanreachageseveraldecadestimebelievedasexuallypropagatedoffspringfoundingroyalpairtermite-funguslonghistorydatingback30millionyearstime-scalelifespanquestionsarisephysicalmoundcolony'slifetimelong-termscalesymbioticraisesquestioninteractionhostsymbiontpersistsgenerationsLongevityColoniesFungus-GrowingTermitesStabilitySymbiosisTermitomycescheatersmutation

Similar Articles

Cited By (9)