Population Dynamics and the Microbiome in a Wild Boreal Mammal: The Snowshoe Hare Cycle and Impacts of Diet, Season and Predation Risk.

Mason R Stothart, Sophia Lavergne, Laura McCaw, Hardeep Singh, Wilfred de Vega, Katherine Amato, Jocelyn Poissant, Rudy Boonstra
Author Information
  1. Mason R Stothart: Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada. ORCID
  2. Sophia Lavergne: Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada.
  3. Laura McCaw: Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada.
  4. Hardeep Singh: Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada.
  5. Wilfred de Vega: Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada.
  6. Katherine Amato: Department of Anthropology, Northwestern University, Evanston, Illinois, USA. ORCID
  7. Jocelyn Poissant: Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada.
  8. Rudy Boonstra: Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada.

Abstract

The North American boreal forest is a massive ecosystem, and its keystone herbivore is the snowshoe hare (Lepus americanus). Hares are exposed to considerable environmental extremes in diet and weather, food availability, and predation risk. Gut microbiomes have been suggested to facilitate adaptive animal responses to environmental change, but severe environmental challenges to homeostasis can also disrupt host-microbiome relationships. To better understand gut microbiome contributions to animal acclimation, we studied the faecal bacterial microbiome of wild hares across two types of extreme environmental change that are integral to their natural history: (1) seasonal transitions between summer and winter, and (2) changes over the ~10���year 'boom-bust' population cycles that are characterised by shifting food resource availability and predation pressure. When compared to summer, hares in winter had lower bacterial richness and were depleted in 20 families (including Oxalobacteraceae and Christensenellaceae) but enriched for Ruminococcaceae (a family which contains plant fibre degrading bacteria) alongside nine other bacterial groups. Marked bacterial microbiome differences also occurred across phases of the population cycle. Bacterial microbiomes were lower in richness and compositionally distinct in the peak compared to the increase or decline phases of the population cycle. Direct measures of host physiology and diet quality (faecal fibre contents) most strongly supported food resource availability as a mechanism underlying phase-based differences in bacterial communities, but faecal fibre contents could not fully account for bacterial microbiome variation across phases.

Keywords

References

  1. ISME J. 2019 Jan;13(1):183-196 [PMID: 30135468]
  2. PLoS One. 2013 Apr 22;8(4):e61217 [PMID: 23630581]
  3. Nat Commun. 2021 Oct 14;12(1):6017 [PMID: 34650048]
  4. Environ Microbiol. 2017 Apr;19(4):1366-1378 [PMID: 28035742]
  5. PeerJ. 2017 Nov 16;5:e4075 [PMID: 29177117]
  6. Curr Opin Biotechnol. 2023 Jun;81:102923 [PMID: 36996728]
  7. Proc Biol Sci. 2019 Apr 24;286(1901):20190431 [PMID: 31014219]
  8. Ecol Evol. 2019 Nov 12;9(23):13202-13217 [PMID: 31871639]
  9. Appl Environ Microbiol. 2013 Sep;79(17):5112-20 [PMID: 23793624]
  10. mSystems. 2018 Mar 6;3(2): [PMID: 29556549]
  11. Sci Rep. 2022 Feb 16;12(1):2605 [PMID: 35173201]
  12. J Anim Ecol. 2006 Jan;75(1):1-13 [PMID: 16903038]
  13. J Chem Ecol. 1988 Jun;14(6):1505-14 [PMID: 24276401]
  14. Front Microbiol. 2024 Jan 11;14:1241259 [PMID: 38274765]
  15. Anim Microbiome. 2021 Jul 5;3(1):46 [PMID: 34225812]
  16. Philos Trans R Soc Lond B Biol Sci. 2020 Sep 28;375(1808):20190589 [PMID: 32772662]
  17. Oecologia. 1986 Sep;70(2):194-197 [PMID: 28311657]
  18. Nucleic Acids Res. 2014 Jan;42(Database issue):D643-8 [PMID: 24293649]
  19. J Anim Ecol. 2009 Nov;78(6):1249-58 [PMID: 19426257]
  20. Nat Biotechnol. 2019 Aug;37(8):953-961 [PMID: 31375809]
  21. Nat Commun. 2020 Jul 14;11(1):3514 [PMID: 32665548]
  22. Trends Ecol Evol. 2016 Sep;31(9):689-699 [PMID: 27453351]
  23. Ecol Lett. 2006 Jun;9(6):683-93 [PMID: 16706913]
  24. Anim Microbiome. 2019 Aug 21;1(1):6 [PMID: 33499955]
  25. Mol Ecol Resour. 2023 Apr;23(3):549-564 [PMID: 36112078]
  26. Science. 2022 Jan 28;375(6579):460-463 [PMID: 35084962]
  27. Nat Microbiol. 2017 Aug 24;2:17121 [PMID: 28836573]
  28. Oecologia. 1984 Mar;61(3):403-410 [PMID: 28311071]
  29. Philos Trans R Soc Lond B Biol Sci. 2020 Sep 28;375(1808):20190597 [PMID: 32772670]
  30. Science. 1995 Aug 25;269(5227):1112-5 [PMID: 17755536]
  31. Ecol Lett. 2022 Apr;25(4):981-991 [PMID: 35148018]
  32. Appl Environ Microbiol. 2007 Aug;73(16):5261-7 [PMID: 17586664]
  33. FEMS Microbiol Ecol. 2023 Oct 17;99(11): [PMID: 37838471]
  34. Bioinformatics. 2006 Nov 15;22(22):2823-4 [PMID: 16982706]
  35. J Anim Ecol. 2018 Jan;87(1):87-100 [PMID: 28636751]
  36. Nat Commun. 2024 Jul 22;15(1):6012 [PMID: 39039075]
  37. mBio. 2018 Jul 31;9(4): [PMID: 30065092]
  38. J Comp Physiol B. 2012 Jan;182(1):139-55 [PMID: 21710385]
  39. Proc Biol Sci. 2019 Oct 23;286(1913):20192111 [PMID: 31640519]
  40. J Comp Physiol B. 2009 Apr;179(3):305-13 [PMID: 18998149]
  41. mSystems. 2015 Dec 22;1(1): [PMID: 27822518]
  42. FEMS Microbiol Ecol. 2020 Jul 1;96(7): [PMID: 32353874]
  43. Am J Physiol Regul Integr Comp Physiol. 2013 Jan 1;304(1):R33-42 [PMID: 23152108]
  44. Mol Ecol. 2018 Apr;27(8):2164-2172 [PMID: 29427300]
  45. PeerJ. 2016 Oct 18;4:e2584 [PMID: 27781170]
  46. BMC Biol. 2019 Oct 28;17(1):83 [PMID: 31660948]
  47. Ecology. 2010 Oct;91(10):2983-94 [PMID: 21058558]
  48. Int J Syst Evol Microbiol. 2012 Jan;62(Pt 1):144-149 [PMID: 21357455]
  49. Science. 2023 Dec 15;382(6676):eadj3502 [PMID: 38096285]
  50. Ecol Evol. 2023 Dec 18;13(12):e10692 [PMID: 38111921]
  51. mSphere. 2017 Mar 8;2(2): [PMID: 28289728]
  52. Appl Environ Microbiol. 1999 Aug;65(8):3738-41 [PMID: 10427077]
  53. Ecology. 2021 Sep;102(9):e03456 [PMID: 34165786]
  54. Science. 2015 Nov 6;350(6261):aac9323 [PMID: 26542581]
  55. PeerJ. 2021 Mar 9;9:e10837 [PMID: 33854827]
  56. PLoS Biol. 2015 Aug 18;13(8):e1002226 [PMID: 26284777]
  57. Nat Rev Microbiol. 2008 Feb;6(2):121-31 [PMID: 18180751]
  58. Microbiome. 2017 Dec 21;5(1):163 [PMID: 29268780]
  59. Oecologia. 2021 Sep;197(1):71-88 [PMID: 34435235]
  60. Nat Ecol Evol. 2022 Jul;6(7):955-964 [PMID: 35654895]
  61. Front Microbiol. 2022 Apr 25;13:809735 [PMID: 35547129]
  62. J Physiol. 2004 Jul 1;558(Pt 1):263-75 [PMID: 15133062]
  63. Glob Chang Biol. 2023 Oct;29(20):5816-5828 [PMID: 37485753]
  64. Proc Natl Acad Sci U S A. 2013 Feb 26;110(9):3229-36 [PMID: 23391737]
  65. Mamm Genome. 2014 Feb;25(1-2):49-74 [PMID: 24281320]
  66. Oecologia. 2014 Nov;176(3):677-89 [PMID: 25270335]
  67. Ecol Lett. 2014 Oct;17(10):1238-46 [PMID: 25040855]
  68. PeerJ. 2022 Mar 15;10:e13095 [PMID: 35310158]
  69. mSystems. 2023 Oct 26;8(5):e0038823 [PMID: 37650612]
  70. Appl Environ Microbiol. 2016 Apr 18;82(9):2669-2675 [PMID: 26896138]

Grants

  1. /Polar Knowledge Canada
  2. /Natural Sciences and Engineering Research Council of Canada

MeSH Term

Animals
Seasons
Diet
Feces
Gastrointestinal Microbiome
Hares
Population Dynamics
Bacteria
Predatory Behavior
Taiga
Microbiota
Ecosystem

Word Cloud

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