The effects of Borrelia infection on its wintering rodent host.
Autumn–winter
Borrelia afzelii
Host–pathogen interactions
Myodes glareolus
Zoonosis
Journal
Oecologia
ISSN: 1432-1939
Titre abrégé: Oecologia
Pays: Germany
ID NLM: 0150372
Informations de publication
Date de publication:
Dec 2022
Dec 2022
Historique:
received:
07
10
2021
accepted:
29
09
2022
pubmed:
16
10
2022
medline:
23
11
2022
entrez:
15
10
2022
Statut:
ppublish
Résumé
In seasonal environments, appropriate adaptations are crucial for organisms to maximize their fitness. For instance, in many species, the immune function has been noticed to decrease during winter, which is assumed to be an adaptation to the season's limited food availability. Consequences of an infection on the health and survival of the host organism could thus be more severe in winter than in summer. Here, we experimentally investigated the effect of a zoonotic, endemic pathogen, Borrelia afzelii infection on the survival and body condition in its host, the bank vole (Myodes glareolus), during late autumn-early winter under semi-natural field conditions in 11 large outdoor enclosures. To test the interaction of Borrelia infection and energetic condition, four populations received supplementary nutrition, while remaining seven populations exploited only natural food sources. Supplementary food during winter increased the body mass independent of the infection status, however, Borrelia afzelii infection did not cause severe increase in the host mortality or affect the host body condition in the late autumn-early winter. While our study suggests that no severe effects are caused by B. afzelii infection on bank vole, further studies are warranted to identify any potentially smaller effects the pathogen may cause on the host fitness over the period of whole winter.
Identifiants
pubmed: 36242620
doi: 10.1007/s00442-022-05272-y
pii: 10.1007/s00442-022-05272-y
pmc: PMC9675652
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
471-478Subventions
Organisme : Academy of Finland
ID : 329332
Organisme : Academy of Finland
ID : 329326
Organisme : Academy of Finland
ID : 320308
Organisme : Academy of Finland
ID : 324605
Organisme : Academy of Finland
ID : 326533
Informations de copyright
© 2022. The Author(s).
Références
Bajer A, Behnke JM, Pawełczyk A, Kuliś K, Sereda MJ, Siński E (2005) Medium-term temporal stability of the helminth component community structure in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology 130:213–228
pubmed: 15727071
doi: 10.1017/S0031182004006389
Barton K (2009) MuMIn: multi-model inference. http://r-forge.r-project.org/projects/mumin/ . Accessed Sept 2022
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
doi: 10.18637/jss.v067.i01
Beldomenico PM, Begon M (2010) Disease spread, susceptibility and infection intensity: vicious circles? Trends Ecol Evol 25:21–27
pubmed: 19782425
doi: 10.1016/j.tree.2009.06.015
Beldomenico PM, Telfer S, Gebert S, Lukomski L, Bennett M, Begon M (2008a) Poor condition and infection: a vicious circle in natural populations. Proc R Soc b Biol Sci 275:1753–1759
doi: 10.1098/rspb.2008.0147
Beldomenico PM, Telfer S, Gebert S, Lukomski L, Bennett M, Begon M (2008b) The dynamics of health in wild field vole populations: a haematological perspective. J Anim Ecol 77:984–997
pubmed: 18564292
pmcid: 2980900
doi: 10.1111/j.1365-2656.2008.01413.x
Bey RF, Loken KI, Wu CC, Lin TL (1995) Experimental infection of the red-backed vole (Clethrionomys gapperi) with Borrelia burgdorferi. J Wildl Dis 31:428–431
pubmed: 8592371
doi: 10.7589/0090-3558-31.3.428
Blanford S, Thomas MB, Pugh C, Pell JK (2002) Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecol Lett 6:2–5
doi: 10.1046/j.1461-0248.2003.00387.x
Boonstra R, Dantzer B, Delehanty B, Fletcher QE, Sheriff MJ (2014) Equipped for life in the boreal forest: the role of the stress axis in mammals. Arctic 67:82–97
doi: 10.14430/arctic4357
Boyce MS (1979) Seasonality and patterns of natural selection for life histories. Am Nat 114:569–583
doi: 10.1086/283503
Bronson FH (2009) Climate change and seasonal reproduction in mammals. Philos Trans R Soc b Biol Sci 364:3331–3340
doi: 10.1098/rstb.2009.0140
Cayol C, Giermek A, Gomez-Chamorro A, Hytönen J, Kallio ER, Mappes T, Salo J, Voordouw MJ, Koskela E (2018) Borrelia afzelii alters reproductive success in a rodent host. Proc R Soc b Biol Sci 285:20181056
doi: 10.1098/rspb.2018.1056
Cichoń M, Chadzińska M, Ksia̧źek A, Konarzewski M (2002) Delayed effects of cold stress on immune response in laboratory mice. Proc R Soc B Biol Sci 269:1493–1497
doi: 10.1098/rspb.2002.2054
Conover DO (1992) Seasonality and the scheduling of life history at different latitudes. J Fish Biol 41:161–178
doi: 10.1111/j.1095-8649.1992.tb03876.x
Demas GE, Nelson RJ (1998) Photoperiod, ambient temperature, and food availability interact to affect reproductive and immune function in adult male deer mice (Peromyscus maniculatus). J Biol Rhythms 13:253–262
pubmed: 9615289
doi: 10.1177/074873098129000093
Eccard JA, Ylönen H (2001) Initiation of breeding after winter in bank voles: effects of food and population density. Can J Zool 79:1743–1753
doi: 10.1139/z01-133
Eriksson M (1984) Winter breeding in three rodent species, the bank vole Clethrionomys glareolus, the yellow-necked mouse Apodemus flavicollis and the wood mouse Apodemus sylvaticus in southern Sweden. Ecography 7:428–429
doi: 10.1111/j.1600-0587.1984.tb01144.x
Forbes KM, Stuart P, Mappes T, Henttonen H, Huitu O (2014) Food resources and intestinal parasites as limiting factors for boreal vole populations during winter. Ecology 95:3139–3148
doi: 10.1890/13-2381.1
Gern L, Schaible UE, Simon MM (1993) Mode of inoculation of the lyme disease agent Borrelia burgdorferi influences infection and immune responses in inbred strains of mice. J Infect Dis 167:971–975
pubmed: 8450262
doi: 10.1093/infdis/167.4.971
Hanincova K, Schäfer SM, Etti S, Sewell HS, Taragelová V, Ziak D, Labuda M, Kurtenbach K (2003) Association of Borrelia afzelii with rodents in Europe. Parasitology 126:11–20
pubmed: 12613759
doi: 10.1017/S0031182002002548
Henttonen H (2000) Long-term dynamics of the bank vole Clethrionomys glareolus at Pallasjärvi, northern Finnish taiga. Pol J Ecol 48:87–96
Huitu O, Jokinen I, Korpimäki E, Koskela E, Mappes T (2007) Phase dependence in winter physiological condition of cyclic voles. Oikos 116:565–577
doi: 10.1111/j.0030-1299.2007.15488.x
Johnsen K, Boonstra R, Boutin S, Devineau O, Krebs CJ, Andreassen HP (2017) Surviving winter: food, but not habitat structure, prevents crashes in cyclic vole populations. Ecol Evol 7:115–124
pubmed: 28070280
doi: 10.1002/ece3.2635
Kallio ER, Voutilainen L, Vapalahti O, Vaheri A, Henttonen H, Koskela E, Mappes T (2007) Endemic hantavirus infection impairs the winter survival of its rodent host. Ecology 88:1911–1916
pubmed: 17824420
doi: 10.1890/06-1620.1
Kane SP (2019) Sample size calculator. https://clincalc.com/stats/samplesize.aspx . Accessed Apr 2022
Kloch A, Baran K, Buczek M, Konarzewski M, Radwan J, Kloch A, Baran ÁK, Buczek ÁM, Radwan ÁJ, Konarzewski M (2013) MHC influences infection with parasites and winter survival in the root vole Microtus oeconomus. Evol Ecol 27:635–653
doi: 10.1007/s10682-012-9611-1
Koskela E, Huitu O, Koivula M, Korpimki E, Mappes T (2004) Sexbiased maternal investment in voles: importance of environmental conditions. Proc R Soc Lond Series B Biol Sci 271:1385–1391
doi: 10.1098/rspb.2004.2711
Kozlowski J (2006) Why life histories are diverse; State-of-the-art review. Pol J Ecol 54:585–605
Ksia̧zek A, Konarzewski M (2012) Effect of dietary restriction on immune response of laboratory mice divergently selected for basal metabolic rate. Physiol Biochem Zool 85:51–61
pubmed: 22237289
doi: 10.1086/663696
Kurtenbach K, Hanincová K, Tsao JI, Margos G, Fish D, Ogden NH (2006) Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat Rev Microbiol 4(9):660–669
pubmed: 16894341
doi: 10.1038/nrmicro1475
Kusumoto K (2009) Effect of food availability on immune function of gray red-backed voles (Myodes rufocanus) exposed to low temperature and short photoperiod. J Mammal 90:416–422
doi: 10.1644/08-MAMM-A-139.1
Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98
doi: 10.1034/j.1600-0706.2000.880110.x
Mannelli A, Bertolotti L, Gern L, Gray J (2012) Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. Oxford Academic, Oxford
Marchand PJ (1996) Life in the cold: an introduction to winter ecology, 3rd edn. University Press of New England, Lebanon
McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15
pubmed: 12614627
doi: 10.1016/S0018-506X(02)00024-7
McNamara JM, Buchanan KL (2005) Stress, resource allocation, and mortality. Behav Ecol 16:1008–1017
doi: 10.1093/beheco/ari087
Mills S, Grapputo A, Jokinen I, Koskela E, Mappes T, Poikonen T (2010) Fitness trade-offs mediated by immunosuppression costs in a small mammal. Evol Int J Org Evol 64:166–179
doi: 10.1111/j.1558-5646.2009.00820.x
Mitchell SE, Rogers ES, Little TJ, Read AF (2005) Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59:70–80
pubmed: 15792228
doi: 10.1111/j.0014-3820.2005.tb00895.x
Moffatt CA, Nelson RJ, Devries AC (1993) Winter adaptations of male deer mice (Peromyscus maniculatus) and Prairie Voles (Microtus ochrogaster) that vary in reproductive responsiveness to photoperiod. J Biol Rhythms 8:221–232
pubmed: 8280911
doi: 10.1177/074873049300800305
Møller AP, Erritzøe J, Saino N (2003) Seasonal changes in immune response and parasite impact on hosts. Am Nat 161:657–671
pubmed: 12778891
doi: 10.1086/367879
Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q R Biol 71:511–548
doi: 10.1086/419555
Oksanen TA, Koskela E, Mappes T (2002) Hormonal manipulation of offspring number: maternal effort and reproductive costs. Evolution 56:1530–1537
pubmed: 12206251
doi: 10.1111/j.0014-3820.2002.tb01463.x
Ostfeld RS, Brisson D, Oggenfuss K, Devine J, Levy MZ, Keesing F (2018) Effects of a zoonotic pathogen, Borrelia burgdorferi, on the behavior of a key reservoir host. Ecol Evol 8:4074–4083
pubmed: 29721281
pmcid: 5916280
doi: 10.1002/ece3.3961
Pedersen AB, Greives TJ (2008) The interaction of parasites and resources cause crashes in a wild mouse population. J Anim Ecol 77:370–377
pubmed: 18028357
doi: 10.1111/j.1365-2656.2007.01321.x
Pinheiro J, Bates D, DebRoy S, Sarkar D (2007) Linear and nonlinear mixed effects models. R Package Version 3:1–89
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ . Accessed Sept 2022
Reil D, Rosenfeld UM, Imholt C, Schmidt S, Ulrich RG, Eccard JA, Jacob J (2017) Puumala hantavirus infections in bank vole populations: host and virus dynamics in Central Europe. BMC Ecol 17:9
pubmed: 28245831
pmcid: 5331674
doi: 10.1186/s12898-017-0118-z
Rizzoli A, Hauffe HC, Carpi G, Vourc’h GI, Neteler M, Rosà R (2011) Lyme borreliosis in Europe. European centre for disease prevention and control. Eurosurveillance 16(27):19906
pubmed: 21794218
doi: 10.2807/ese.16.27.19906-en
Salo J, Jaatinen A, Söderström M, Viljanen M, Hytönen J (2015) Decorin binding proteins of Borrelia burgdorferi promote arthritis development and joint specific post-treatment DNA persistence in mice. PLoS ONE 10(3):e0121512
pubmed: 25816291
pmcid: 4376631
doi: 10.1371/journal.pone.0121512
Scholthof KBG (2007) The disease triangle: pathogens, the environment and society. Nat Rev Microbiol 5:152–156
pubmed: 17191075
doi: 10.1038/nrmicro1596
Schroderus E, Jokinen I, Koivula M, Koskela E, Mappes T, Mills SC, Oksanen TA, Poikonen T (2015) Intra- and intersexual trade-offs between testosterone and immune system: implications for sexual and sexually antagonistic selection. Am Nat 176:E90–E97
doi: 10.1086/656264
Schwanz LE, Voordouw MJ, Brisson D, Ostfeld RS (2011) Borrelia burgdorferi has minimal impact on the lyme disease reservoir host peromyscus leucopus. Vector-Borne Zoonotic Dis 11:117–124
pubmed: 20569016
doi: 10.1089/vbz.2009.0215
Sipari S, Haapakoski M, Klemme I, Palme R, Sundell J, Ylönen H (2016) Population sex-ratio affecting behavior and physiology of overwintering bank voles (Myodes glareolus). Physiol Behav 159:45–51
pubmed: 26976741
doi: 10.1016/j.physbeh.2016.03.008
Stanek G, Wormser GP, Gray J, Strle F (2012) Lyme borreliosis. Elsevier B.V, Amsterdam
Stearns S (1992) The evolution of life histories. Oxford University Press, Oxford, p 249
Svensson E, Råberg L, Koch C, Hasselquist D (1998) Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12:912–919
doi: 10.1046/j.1365-2435.1998.00271.x
Telfer S, Bennett M, Bown K, Cavanagh R, Crespin L, Hazel S, Jones T, Begon M (2002) The effects of cowpox virus on survival in natural rodent populations: increases and decreases. J Anim Ecol 71:558–568
doi: 10.1046/j.1365-2656.2002.00623.x
Tersago K, Crespin L, Verhagen R, Leirs H (2012) Impact of Puumala virus infection on maturation and survival in bank voles: a capture-mark-recapture analysis. J Wildl Dis 48:148–156
pubmed: 22247383
doi: 10.7589/0090-3558-48.1.148
Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parasitol Today 15(8):311–313
pubmed: 10407375
doi: 10.1016/S0169-4758(99)01484-2
Tompkins DM, Dobson AP, Arneberg P, Begon M, Cattadori I, Greenman J, Heesterbeek J, Hudson P, Newborn D, Pugliese A, Rizzoli A, Rosa R, Rosso F, Wilson K (2001) Parasites and host population dynamics. The Ecology of Wildlife Diseases. Oxford University Press, Oxford, pp 45–62
Van Cann J, Koskela E, Mappes T, Mikkonen AM, Mokkonen M, Watts PC (2019) Early life of fathers affects offspring fitness in a wild rodent. J Evol Biol 32:1141–1151
pubmed: 31390473
doi: 10.1111/jeb.13516
Varpe Ø (2017) Life history adaptations to seasonality. Integrative and Comparative Biology. Oxford University Press, Oxford, pp 943–960
Von Blanckenhagen F, Eccard JA, Ylönen H (2007) Animal protein as a reproductive constraint in spring reproduction of the bank vole. Ecoscience 14:323–329
doi: 10.2980/1195-6860(2007)14[323:APAARC]2.0.CO;2
Voordouw MJ, Lachish S, Dolan MC (2015) The lyme disease pathogen has no effect on the survival of its rodent reservoir host. PLoS ONE 10:e0118265
pubmed: 25688863
pmcid: 4331372
doi: 10.1371/journal.pone.0118265
Ylönen H, Eccard JA (2004) Does quality of winter food affect spring condition and breeding in female bank voles (Clethrionomys glareolus)? Ecoscience 11:1–5
doi: 10.1080/11956860.2004.11682803
Yrjänäinen H, Hytönen J, Söderström KO, Oksi J, Hartiala K, Viljanen MK (2006) Persistent joint swelling and borrelia-specific antibodies in Borrelia garinii-infected mice after eradication of vegetative spirochetes with antibiotic treatment. Microbes Infect 8:2044–2051
pubmed: 16797205
doi: 10.1016/j.micinf.2006.03.008