Abolins, S. et al. The comparative immunology of wild and laboratory mice, Mus musculus domesticus. Nat. Commun. 8, 14811. https://doi.org/10.1038/ncomms14811 (2017).
Google Scholar
Cox, F. E. G. Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38. https://doi.org/10.1017/S003118200001698X (2001).
Google Scholar
Seder, R. A., Darrah, P. A. & Roederer, M. T-cell quality in memory and protection: Implications for vaccine design. Nat. Rev. Immunol. 8, 247–258. https://doi.org/10.1038/nri2274 (2008).
Google Scholar
Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P. & French, S. S. Beyond phytohaemagglutinin: Assessing vertebrate immune function across ecological contexts. J. Anim. Ecol. 80, 710–730. https://doi.org/10.1111/j.1365-2656.2011.01813.x (2011).
Google Scholar
Pedersen, A. B. & Babayan, S. A. Wild immunology. Mol. Ecol. 20, 872–880. https://doi.org/10.1111/j.1365-294X.2010.04938.x (2011).
Google Scholar
Abolins, S. et al. The ecology of immune state in a wild mammal, Mus musculus domesticus. PLoS Biol. 16, e2003538. https://doi.org/10.1371/journal.pbio.2003538 (2018).
Google Scholar
Ezenwa, V. O. Helminth–microparasite co-infection in wildlife: Lessons from ruminants, rodents and rabbits. Parasite Immunol. 38, 527–534. https://doi.org/10.1111/pim.12348 (2016).
Google Scholar
Craig, B. H., Tempest, L. J., Pilkington, J. G. & Pemberton, J. M. Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology 135, 433–441. https://doi.org/10.1017/S0031182008004137 (2008).
Google Scholar
Graham, A. L. et al. Exposure to viral and bacterial pathogens among Soay sheep (Ovis aries) of the St Kilda archipelago. Epidemiol. Infect. 144, 1879–1888. https://doi.org/10.1017/S0950268816000017 (2016).
Google Scholar
Murphy, K., Travers, P., Walport, M. & Janeway, C. Janeway’s Immunobiology (Garland Science, 2012).
Parkin, J. & Cohen, B. An overview of the immune system. Lancet 357, 1777–1789. https://doi.org/10.1016/S0140-6736(00)04904-7 (2001).
Google Scholar
Mosmann, T. R. & Coffman, R. L. TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7, 145–173. https://doi.org/10.1146/annurev.iy.07.040189.001045 (1989).
Google Scholar
Nakayamada, S., Takahashi, H., Kanno, Y. & O’Shea, J. J. Helper T cell diversity and plasticity. Curr. Opin. Immunol. 24, 297–302. https://doi.org/10.1016/j.coi.2012.01.014 (2012).
Google Scholar
Gerbe, F. et al. Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature 529, 226–230. https://doi.org/10.1038/nature16527 (2016).
Google Scholar
Jain, A. & Pasare, C. Innate control of adaptive immunity: Beyond the three-signal paradigm. J. Immunol. (Baltimore, Md.: 1950) 198, 3791–3800. https://doi.org/10.4049/jimmunol.1602000 (2017).
Google Scholar
Schmitt, N. & Ueno, H. Regulation of human helper T cell subset differentiation by cytokines. Curr. Opin. Immunol. 34, 130–136. https://doi.org/10.1016/j.coi.2015.03.007 (2015).
Google Scholar
Abbas, A. K., Murphy, K. M. & Sher, A. Functional diversity of helper T lymphocytes. Nature 383, 787–793. https://doi.org/10.1038/383787a0 (1996).
Google Scholar
Seder, R. A. & Paul, W. E. Acquisition of lymphokine-producing phenotype by CD4+ T cells. Annu. Rev. Immunol. 12, 635–673. https://doi.org/10.1146/annurev.iy.12.040194.003223 (1994).
Google Scholar
Grencis, R. K. Immunity to helminths: Resistance, regulation, and susceptibility to gastrointestinal nematodes. Annu. Rev. Immunol. 33, 201–225. https://doi.org/10.1146/annurev-immunol-032713-120218 (2015).
Google Scholar
O’Garra, A. & Robinson, D. In Advances in Immunology vol. 83 133–162 (Academic Press, 2004).
Pereira, L. M. S., Gomes, S. T. M., Ishak, R. & Vallinoto, A. C. R. Regulatory T cell and forkhead box protein 3 as modulators of immune homeostasis. Front. Immunol. https://doi.org/10.3389/fimmu.2017.00605 (2017).
Google Scholar
Romagnani, S. T-cell subsets (Th1 versus Th2). Ann. Allergy Asthma Immunol. 85, 9–21. https://doi.org/10.1016/S1081-1206(10)62426-X (2000).
Google Scholar
Sandquist, I. & Kolls, J. Update on regulation and effector functions of Th17 cells. F1000Res 7, 205–205. https://doi.org/10.12688/f1000research.13020.1 (2018).
Google Scholar
Stockinger, B. & Omenetti, S. The dichotomous nature of T helper 17 cells. Nat. Rev. Immunol. 17, 535–544. https://doi.org/10.1038/nri.2017.50 (2017).
Google Scholar
Wilson, K., Fenton, A. & Tompkins, D. Wildlife Disease Ecology: Linking Theory to Data and Application (Cambridge University Press, 2019).
Google Scholar
Graham, A. L. Ecological rules governing helminth–microparasite coinfection. PNAS 105, 566–570. https://doi.org/10.1073/pnas.0707221105 (2008).
Google Scholar
Ezenwa, V. O., Etienne, R. S., Luikart, G., Beja-Pereira, A. & Jolles, A. E. Hidden consequences of living in a wormy world: Nematode-induced immune suppression facilitates tuberculosis invasion in African Buffalo. Am. Nat. 176, 613–624. https://doi.org/10.1086/656496 (2010).
Google Scholar
Ezenwa, V. O. & Jolles, A. E. Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science 347, 175–177. https://doi.org/10.1126/science.1261714%JScience (2015).
Google Scholar
Arriero, E. et al. From the animal house to the field: Are there consistent individual differences in immunological profile in wild populations of field voles (Microtus agrestis)?. PLoS One 12, e0183450. https://doi.org/10.1371/journal.pone.0183450 (2017).
Google Scholar
Jackson, J. A. et al. An immunological marker of tolerance to infection in wild rodents. PLoS Biol. 12, e1001901. https://doi.org/10.1371/journal.pbio.1001901 (2014).
Google Scholar
Beirne, C., Delahay, R. & Young, A. Sex differences in senescence: The role of intra-sexual competition in early adulthood. Proc. R. Soc. B. 282, 20151086. https://doi.org/10.1098/rspb.2015.1086 (2015).
Google Scholar
Young, S. et al. Relationships between immune gene expression and circulating cytokine levels in wild house mice. Ecol. Evol. 10, 13860–13871. https://doi.org/10.1002/ece3.6976 (2020).
Google Scholar
Turner, J. D. et al. Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J. Infect. Dis. 188, 1768–1775. https://doi.org/10.1086/379370 (2003).
Google Scholar
Craig, B. H., Pilkington, J. G., Kruuk, L. E. B. & Pemberton, J. M. Epidemiology of parasitic protozoan infections in Soay sheep (Ovis aries L.) on St Kilda. Parasitology 134, 9–21. https://doi.org/10.1017/S0031182006001144 (2006).
Google Scholar
Maizels, R. M., Hewitson, J. P. & Smith, K. A. Susceptibility and immunity to helminth parasites. Curr. Opin. Immunol. 24, 459–466. https://doi.org/10.1016/j.coi.2012.06.003 (2012).
Google Scholar
Ozmen, O., Adanir, R. & Haligur, M. Immunohistochemical detection of the cytokine and chemokine expression in the gut of lambs and kids with coccidiosis. Small Rumin. Res. 105, 345–350. https://doi.org/10.1016/j.smallrumres.2011.11.010 (2012).
Google Scholar
Woolhouse, M. E. J. Patterns in parasite epidemiology: The peak shift. Parasitol. Today 14, 428–434. https://doi.org/10.1016/S0169-4758(98)01318-0 (1998).
Google Scholar
Gibson, T. E. & Parfitt, J. W. The effect of age on the development by sheep of resistance to Trichostrongylus colubriformis. Res. Vet. Sci. 13, 529–535 (1972).
Google Scholar
Smith, W. D., Jackson, F., Jackson, E. & Williams, J. Age immunity to Ostertagia circumcincta: Comparison of the local immune responses of 4 1/2- and 10-month-old lambs. J. Comp. Pathol. 95, 235–245. https://doi.org/10.1016/0021-9975(85)90010-6 (1985).
Google Scholar
Peters, A., Delhey, K., Nakagawa, S., Aulsebrook, A. & Verhulst, S. Immunosenescence in wild animals: Meta-analysis and outlook. Ecol. Lett. 22, 1709–1722. https://doi.org/10.1111/ele.13343 (2019).
Google Scholar
Sparks, A. M. et al. Natural selection on antihelminth antibodies in a wild mammal population. Am. Nat. 192, 745–760. https://doi.org/10.1086/700115 (2018).
Google Scholar
Froy, H. et al. Senescence in immunity against helminth parasites predicts adult mortality in a wild mammal. Science 365, 1296–1298. https://doi.org/10.1126/science.aaw5822%JScience (2019).
Google Scholar
Nussey, D. H., Watt, K., Pilkington, J. G., Zamoyska, R. & McNeilly, T. N. Age-related variation in immunity in a wild mammal population. Aging Cell 11, 178–180. https://doi.org/10.1111/j.1474-9726.2011.00771.x (2012).
Google Scholar
Watson, R. L. et al. Cellular and humoral immunity in a wild mammal: Variation with age & sex and association with overwinter survival. Ecol. Evol. 6, 8695–8705. https://doi.org/10.1002/ece3.2584 (2016).
Google Scholar
Pennock, N. D. et al. T cell responses: Naive to memory and everything in between. Adv. Physiol. Educ. 37, 273–283. https://doi.org/10.1152/advan.00066.2013 (2013).
Google Scholar
Chipeta, J. et al. CD4+and CD8+Cell cytokine profiles in neonates, older children, and adults: Increasing T helper type 1 and T cytotoxic type 1 cell populations with age. Cell. Immunol. 183, 149–156. https://doi.org/10.1006/cimm.1998.1244 (1998).
Google Scholar
Sakata-Kaneko, S., Wakatsuki, Y., Matsunaga, Y., Usui, T. & Kita, T. Altered Th1/Th2 commitment in human CD4+ T cells with ageing. Clin. Exp. Immunol. 120, 267–273. https://doi.org/10.1046/j.1365-2249.2000.01224.x (2000).
Google Scholar
Duddy, M. E., Alter, A. & Bar-Or, A. Distinct profiles of human B cell effector cytokines: A role in immune regulation?. J. Immunol. (Baltimore, Md.: 1950) 172, 3422–3427. https://doi.org/10.4049/jimmunol.172.6.3422 (2004).
Google Scholar
Varma, T. K., Lin, C. Y., Toliver-Kinsky, T. E. & Sherwood, E. R. Endotoxin-induced gamma interferon production: Contributing cell types and key regulatory factors. Clin. Diagn. Lab. Immunol. 9, 530–543. https://doi.org/10.1128/CDLI.9.3.530-543.2002 (2002).
Google Scholar
McNeilly, T. N. et al. Suppression of ovine lymphocyte activation by Teladorsagia circumcincta larval excretory-secretory products. Vet. Res. 44, 70. https://doi.org/10.1186/1297-9716-44-70 (2013).
Google Scholar
Restif, O. & Amos, W. The evolution of sex-specific immune defences. Proc. R. Soc. B Biol. Sci. 277, 2247–2255. https://doi.org/10.1098/rspb.2010.0188 (2010).
Google Scholar
Hayward, A. D. et al. Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics. Am. Nat. 184, S58–S76. https://doi.org/10.1086/676929 (2014).
Google Scholar
Sparks, A. M. et al. The genetic architecture of helminth-specific immune responses in a wild population of Soay sheep (Ovis aries). PLoS Genet. 15, e1008461. https://doi.org/10.1371/journal.pgen.1008461 (2019).
Google Scholar
Hayward, A. D., Wilson, A. J., Pilkington, J. G., Pemberton, J. M. & Kruuk, L. E. B. Ageing in a variable habitat: Environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proc. R. Soc. B. 276, 3477–3485. https://doi.org/10.1098/rspb.2009.0906 (2009).
Google Scholar
Mosmann, T. R. & Sad, S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol. Today 17, 138–146. https://doi.org/10.1016/0167-5699(96)80606-2 (1996).
Google Scholar
Hassan, M., Hanrahan, J. P., Good, B., Mulcahy, G. & Sweeney, T. A differential interplay between the expression of Th1/Th2/Treg related cytokine genes in Teladorsagia circumcincta infected DRB1*1101 carrier lambs. Vet. Res. 42, 45. https://doi.org/10.1186/1297-9716-42-45 (2011).
Google Scholar
Noordwijk, A. J. V. & Jong, G. D. Acquisition and allocation of resources: Their influence on variation in life history tactics. Am. Nat. 128, 137–142. https://doi.org/10.1086/284547 (1986).
Google Scholar
Grainger, J. R. et al. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J. Exp. Med. 207, 2331–2341. https://doi.org/10.1084/jem.20101074 (2010).
Google Scholar
Smith, K. A. et al. Low-level regulatory T-cell activity is essential for functional type-2 effector immunity to expel gastrointestinal helminths. Mucosal Immunol. 9, 428–443. https://doi.org/10.1038/mi.2015.73 (2016).
Google Scholar
Beirne, C., Waring, L., McDonald, R. A., Delahay, R. & Young, A. Age-related declines in immune response in a wild mammal are unrelated to immune cell telomere length. Proc. R. Soc. B. 283, 20152949. https://doi.org/10.1098/rspb.2015.2949 (2016).
Google Scholar
Zaros, L. G. et al. Response of resistant and susceptible Brazilian Somalis crossbreed sheep naturally infected by Haemonchus contortus. Parasitol. Res. 113, 1155–1161. https://doi.org/10.1007/s00436-014-3753-8 (2014).
Google Scholar
Gossner, A., Wilkie, H., Joshi, A. & Hopkins, J. Exploring the abomasal lymph node transcriptome for genes associated with resistance to the sheep nematode Teladorsagia circumcincta. Vet. Res. 44, 68. https://doi.org/10.1186/1297-9716-44-68 (2013).
Google Scholar
Wilkie, H., Gossner, A., Bishop, S. & Hopkins, J. Variations in T cell transcription factor sequence and expression associated with resistance to the sheep nematode Teladorsagia circumcincta. PLoS One 11, e0149644. https://doi.org/10.1371/journal.pone.0149644 (2016).
Google Scholar
Nussey, D. H., Coulson, T., Festa-Bianchet, M. & Gaillard, J.-M. Measuring senescence in wild animal populations: Towards a longitudinal approach. Funct. Ecol. 22, 393–406. https://doi.org/10.1111/j.1365-2435.2008.01408.x (2008).
Google Scholar
Seguel, M. et al. Immune stability predicts tuberculosis infection risk in a wild mammal. Proc. Biol. Sci. 286, 20191401. https://doi.org/10.1098/rspb.2019.1401 (2019).
Google Scholar
Pemberton, J. M. & Clutton-Brock, T. H. Soay Sheep: Dynamics and Selection in an Island Population (Cambridge University Press, 2004).
Corripio-Miyar, Y. et al. Phenotypic and functional analysis of monocyte populations in cattle peripheral blood identifies a subset with high endocytic and allogeneic T-cell stimulatory capacity. Vet. Res. 46, 112. https://doi.org/10.1186/s13567-015-0246-4 (2015).
Google Scholar
Kwong, L. S. et al. Development of an ELISA for bovine IL-10. Vet. Immunol. Immunopathol. 85, 213–223. https://doi.org/10.1016/S0165-2427(02)00007-7 (2002).
Google Scholar
Wattegedera, S. R. et al. Enhancing the toolbox to study IL-17A in cattle and sheep. Vet. Res. 48, 20–20. https://doi.org/10.1186/s13567-017-0426-5 (2017).
Google Scholar
Jackson, F. New technique for obtaining nematode ova from sheep faeces. Lab. Pract. 23, 65–66 (1974).
Google Scholar
R Development Core Team. R: A language and environment for statistical computing. Accessed Feb 2020. https://www.R-project.org/ (2019).
Venables, W. N. & Ripley, B. D. Random and Mixed Effects. In Modern Applied Statistics with S. Statistics and Computing. (2002).
Package “corrplot”: visualization of a correlation matrix v. (Version 0.84) (2017).
Jari Oksanen, F. et al. vegan: Community Ecology Package. R package version 2.5-6. Accessed Feb 2020. https://CRAN.R-project.org/package=vegan (2019).
Source: Ecology - nature.com