Jump to content

Ecoimmunology

Add links
From Wikipedia, the free encyclopedia

This is an old revision of this page, as edited by Headbomb (talk | contribs) at 06:57, 14 July 2022 (→Body size: | Alter: journal. | Use this tool. Report bugs. | #UCB_Gadget). The present address (URL) is a permanent link to this revision, which may differ significantly from the current revision.

Ecoimmunology or Ecological Immunology is the study of the causes and consequences of variation in immunity.[1][2] The field of ecoimmunology seeks to give an ultimate perspective for proximate mechanisms of immunology. This approach places immunology in evolutionary and ecological contexts across all levels of biological organization.

Classical, or mainstream, immunology works hard to control variation (inbred/domestic model organisms, parasite-free environments, etc.) and asks questions about mechanisms and functionality of the immune system using a reductionist method. While ecoimmunology originated from these fields, it is distinguished by its focus to explain natural variation in immune functions.[3]

Multiple institutes engage in ecoimmunological research, such as the Center for Immunity, Infection and Evolution at the University of Edinburgh and the Max Planck Institute for Immunoecology and Migration. The US National Science Foundation has funded a Research Coordination Network) to bring methodological and conceptual unity to the field of ecoimmunology. The causes and consequences of immune variation have larger implications for public health, conservation, wildlife management, and agriculture.[4]

History

Ecological Immunology is a discipline that uses ecological perspectives to understand variation in immune function. Specifically to explain how abiotic and biotic factors influence the variation in immune function.[3] Articles began discussing ecological contexts and of immune variation in the 1970s but matured into a discipline in the 1990s.[5] Ecoimmunology is an integrative field that combines approaches from evolutionary biology, ecology, neurobiology, and endocrinology.[6]

Seminal papers

Seminal papers in the field include Sheldon & Verhulst's [3] which proposed concepts from Life history theory, trade-offs and allocation of resources between competing costly physiological functions, are a cause of variation in immunity [5] One of the field’s seminal papers, by Folstad and Karter,[7] was a response to Hamilton and Zuk’s famous paper on the handicap hypothesis for sexually selected traits.[8] Folstad and Karter proposed the immunocompetence handicap hypothesis, whereby testosterone acts as a mediator of immunosuppression and thus keeps sexually-selected traits honest.[7] Although there is only moderate observational or experimental evidence supporting this claim up until now, the paper itself was one of the first links to be made suggesting a cost to immunity requiring trade-offs between it and other physiological processes.

More recently, ecoimmunology has been the theme of three special issues in peer-reviewed journals, in Philosophical Transactions of the Royal Society B, in Functional Ecology, and in Physiological and Biochemical Zoology (see External links).

Known factors that influence immune variation

Intraspecific constraints

Organisms allocate energy between competing processes including self-maintenance, reproduction, or growth.[9] Energy availability is limited, and the resources used for one of the competing metabolic tasks (i.e., growth, immune response) cannot be directed towards another.[10] The cost of immunity is central to the understanding of ecoimmunology. Natural selection should favor the optimal immune response that maximizes total lifetime reproductive output. The costs of immunity to parasites occur at the individual and the evolutionary scale.[1] Trade-offs between bodily demands are titrated in relation to the local and social ecology.[11]

Innnate versus acquired

One axis on which these trade-offs occur is the trade-off between innate and acquired immunity. McDade applies a framework that considers three ecological factors that shape life-history trade-offs.[12] The framework suggests that environments with high extrinsic mortality should favor innate immunity or short-term immunity while low extrinsic mortality should allow for a longer time horizon in order to invest in acquired or long-term immunity.[12]

  • The availability of nutritional resources
  • The intensity of pathogen exposure
  • Signals of extrinsic mortality risk

Childhood growth

Among organisms, in developmental stages, the allocation of energy toward immune function may trade-off with physical growth, particularly in environments characterized by high-pathogen and low resources.[13] In Tsimane children, a 49% reduction in growth was observed in children with mild immune activation.[14]

Body size

Body size affects the extent to which an organism is exposed to parasites as well as limitations on how organisms can mount an immune response.[4] A meta-analysis across animal taxa found that small animals, disproportionately long-lived for their size, experience the largest costs of immune activation.[15]

Reproduction

Physiological and behavioral changes during reproduction are known to influence the immune system.[16] Trade-offs occur between bodily maintenance (which includes immune function) and reproduction, as metabolic energy expenditure is increased during pregnancy and lactation.[17] The reproductive system is unique in that its function is to produce offspring while the immune system provides internal protection.[18] Both systems are regulated by chemical signals in response to environmental stimuli and rely on interactions between both systems in order for each to function properly.[18] Increased parasitism in animals during reproductive phases has been well documented,[19][20][21] however it is unclear if changes in the immune system are causing this as few studies include measures for both immunity and parasitism.[22] A study of wild red deer on the Isle of Rum, off the coast of Scotland, found that reproducing females had lower antibody levels and higher parasite counts.[22] In humans, life history events such as menarche may be delayed and menopause sped up by infectious disease.[23]

Testosterone

The Immunocompetence Handicap Hypothesis and similar theories propose that testosterone mediates a trade-off between longevity and reproductive effort in males, prioritizing investment in secondary sexual characteristics such as sexually dimorphic muscle mass.[7][24] Energetically expensive secondary sexual characteristics, such as skeletal muscle mass, have been shown to predict a relationship between testosterone levels and reproductive effort.[25]

Human males experience muscle mass deterioration during times of immunological and nutritional stress.[24][25] In humans, studies have reported lower testosterone in males with acute illnesses, including sepsis, surgery[26]  and HIV.[27]

A different theoretical model has been proposed for testosterone variability as phenotypic plasticity taking into account behavioral and environmental impacts as well as the role of immune activation on testosterone levels.[25] This model considers the variability we see as a plastic response to environmental stimuli and disease risk in different ecological environments, fundamental shifts between energetic allocations from reproductive to somatic efforts. Within this framework, lowered testosterone in response to injury or illness may be indicative of an adaptive response.[25]

Stress and cortisol

Stress through the release of stress hormones, such as glucocorticoids, influence immune function. Glucocorticoids, like cortisol stimulates mobilization of glucose when energetic demands are increased.[6] Psychological stress responses that trigger physiological changes in organisms in order to cope with the stress modulate immune responses.[28] Activation of the hypothalamic-pituitary adrenal (HPA) axis is one of the main mechanisms by which the immune system interacts with stress.[29] In animal studies, stressors such as social disruption and restraint stress active HPA axis in mice[29] In both human and animal models, studies have shown that varying times of stress can reactivate latent HSV-1.[29] Stress have been shown to increase ocular shedding of HSV-1 shedding in mice [30] and nasal shedding in bovine.[31] In humans, stress is a predictor of recurrences of herpes simplex virus outbreaks [32] and Epstein-Barr virus.[33]

Interactions with parasites

Host feeding behavior

Parasite-altered feeding behaviors have been observed in several species.[34][35][36][37][38] Most studies conclude that there is a fitness benefit of altering host feeding behavior to either the host or the parasite. The species S.littoralis caterpillar when infected with nucleopolyhedrovirus will self-select a protein-rich diet, which increases its probability of survival.[39]

Parasite manipulation

Selection is expected to favor parasite manipulation of the host when the host’s behavior creates a suboptimal environment for the parasite’s fitness.[40]  An application of coevolutionary theory would predict sophisticated manipulations of host behavior when host-specificity is high.[40] Manipulation must be distinguished from disruption or dysfunction, as such experiments must demonstrate that parasite-altered behavior has fitness benefits for the parasite and that it is regulated or controlled physiologically by the parasite.[40]

Host resistance

Self-medication, a form of host resistance, is defined as an individual response to infection through the ingestion or harvesting of non-nutritive compounds or plant materials.[41] This phenomenon has been observed in several species, with the most prominent examples including the ingestion of whole leaves by primate species to reduce nematode infections and the ingestion of secondary plant metabolites by caterpillars and bumblebees.[42][43][44][39][45] In social insects, behaviors that reduce colony-level parasite loads are termed “social immunity”.[46] An example of this, Apis mellifera incorporate plant resins in their nest building as this can reduce the chronic elevation of an immune response at the individual level.[41] High activation of immunity imposes fitness costs both at the individual and colony level, thus social immunity reduced individual and colony level costs.

Additional Interactions

Nutritional stress

The upregulation of the immune system incurs significant nutritional costs in the forms of protein and energy.[47] Immune costs are often seen when organisms are in stressful environments [48] such as experiencing nutritional stress. In animal models, fruit flies that were selected for parasitoid resistance showed reduced larval competitiveness only when they were subject to food limitations.[48][49]

Leptin has been proposed as a mediator of energetic trade-offs, as a potential provider of signal for current energy availability.[50]

Microbiome

Rapid changes in the gut microbiome occurred during human evolution[51] Because the microbiome is influenced by the host environment, researchers believe that it played a role in facilitating human adaptation to novel environments facilitated through periods of climate change and migration.[52] For instance, commensal microbes influence the host’s ability to survive pathogenic exposures through several mechanisms including inter-microbial competition and interaction with the immune system.[52] In humans, the microbiome also contributes to many bodily functions such as nutrient processing and fat regulation.[48]

Seasonality

Seasonal changes in immunity arise in wildlife populations due to changes in disease threats over time and trade-offs between immune function and other seasonally variable investments such as reproductive efforts.[5] Examples of these costly reproductive efforts include molting, thermoregulation, and migration in birds.[5] Seasonal immunosuppression is seen during long days in summer among reptiles and birds.[16]

Temperature stress

Temperature stress has been causally linked to declines in immune function in several species including C. elegans, Daphnia magna, and Drosophila melanogaster.[48] Cold stress has been shown to inhibit phagocity in macrophages in mice.[53]

Population genetics

Population genetic characteristics such as population size, mutation frequency, and selective processes are important host-parasite co-evolutionary dynamics and therefore influence the evolution of different aspects of the immune system.[48]

Pathogen stress is a major recent selection pressure in human evolution.[54] Pathogen-driven selection has been supported in allele frequency studies including MHC I and blood group antigens.[55] Gene networks have also been correlated with specific pathogens including helminths.[55]

Studies have shown genes that are differently expressed based on genetic ancestry shape interindividual variation of immune cell responses to viral infections, but most of these effects are cell type-specific.[54] Segments of Neanderthal ancestry genomes introgressed to modern humans are enriched for proteins that interact with viruses suggestive of viral selection pressure throughout evolution.[56]

Critiques

Early studies in ecoimmunology tended to underestimate the complexities of parasite defenses, often relying on one or two immune metrics as an overall indication of anti-pathogen defense capabilities.[4] Many studies involve in vivo laboratory experiments, but there have been recent calls for immunologists to study immune variation more in wild animals in particular.[57] To date, sampling wild populations have shown there is substantial inter-individual immune variation.[6]

Another source of criticism comes from the need for to develop assays that can be utilized across species and be accessible in multiple laboratories due to the fact that ecoimmunologists primarily study non-model organisms.[6]

Evolutionary implications

Ecoimmunology allows for the incorporation of more realistic details of variation in individual immune responses in a population. New research has demonstrated that individual variation in infectiousness follows a highly skewed distribution, with very few individuals being highly infectious.[58] Models that account for heterogeneity, predicted rare more rapidly-spreading epidemics and argued for the use of different types of public health interventions compared to models that assume a normal distribution of variation in infectiousness.[58]

Models of host-pathogen coevolution have shown that the nature of life-history trade-offs can greatly alter the evolution of pathogen virulence and its ability to harm infected hosts.[59]

Recent advances in theoretical modeling have allowed for the increased integration of within-organism processes (such as immune-mediated reduction in pathogen replication) and between organism processes (such as transmission).[58] For example, by modeling both host immune defenses and within-host evolution of the Hepatitis C virus, showed that cross-reactivity of immune responses can be a crucial determinant of the chronicity of infection and the probability of transmission.[60]

Medical implications

One of the most influential contributions of ecoimmunology has been the concept of tolerance which incorporates the cost of infection into measures of immunity. The study of tolerance has implications in human biomedicine, wildlife ecology, and public health.[4] For example, there has been growing interest in the "antibiotic crisis" caused by the increased prevalence of drug-resistant microbes and a decline in the discovery of new antibiotic treatments.[61] A shift in focus to tolerance rather than eradication might provide fruitful avenues for treatments that reduce virulence rather than eliminating parasites.[62][63][64]

See also

References

  1. ^ a b Brock PM, Murdock CC, Martin LB (September 2014). "The history of ecoimmunology and its integration with disease ecology". Integrative and Comparative Biology. 54 (3): 353–362. doi:10.1093/icb/icu046. PMC 4184350. PMID 24838746.
  2. ^ Downs C (June 2014). "A primer in ecoimmunology and immunology for wildlife research and management". California Fish and Game. 100: 371–395.
  3. ^ a b c Sheldon BC, Verhulst S (August 1996). "Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology". Trends in Ecology & Evolution. 11 (8): 317–321. doi:10.1016/0169-5347(96)10039-2. PMID 21237861.
  4. ^ a b c d Schoenle LA, Downs CJ, Martin LB (2018). "An Introduction to Ecoimmunology". In Cooper EL (ed.). Advances in Comparative Immunology. Cham: Springer International Publishing. pp. 901–932. doi:10.1007/978-3-319-76768-0_26. ISBN 978-3-319-76767-3. PMC 7114998.
  5. ^ a b c d Martin LB, Hawley DM (2011). Ardia DR (ed.). "An introduction to ecological immunology". Functional Ecology. 25: 1–4. doi:10.1111/j.1365-2435.2010.01820.x.
  6. ^ a b c d Demas GE, Carlton ED (February 2015). "Ecoimmunology for psychoneuroimmunologists: Considering context in neuroendocrine-immune-behavior interactions". Brain, Behavior, and Immunity. 44: 9–16. doi:10.1016/j.bbi.2014.09.002. PMC 4275338. PMID 25218837.
  7. ^ a b c Folstad I, Karter AJ (1992). "Parasites, bright males, and the immunocompetence handicap". American Naturalist. 139 (3): 603–22. doi:10.1086/285346. JSTOR 2462500. S2CID 85266542.
  8. ^ Hamilton WD, Zuk M (October 1982). "Heritable true fitness and bright birds: a role for parasites?". Science. 218 (4570): 384–387. Bibcode:1982Sci...218..384H. doi:10.1126/science.7123238. PMID 7123238.
  9. ^ Hill K, Kaplan H (October 1999). "Life history traits in humans: theory and empiricial studies". Annual Review of Anthropology. 28 (1): 397–430. doi:10.1146/annurev.anthro.28.1.397. PMID 12295622.
  10. ^ McDade TW (October 2005). "The ecologies of human immune function". Annual Review of Anthropology. 34 (1): 495–521. doi:10.1146/annurev.anthro.34.081804.120348. ISSN 0084-6570.
  11. ^ McDade TW (2003). "Life history theory and the immune system: steps toward a human ecological immunology". American Journal of Physical Anthropology. 122 (Suppl 37): 100–125. doi:10.1002/ajpa.10398. PMID 14666535.
  12. ^ a b McDade TW, Georgiev AV, Kuzawa CW (2016). "Trade-offs between acquired and innate immune defenses in humans". Evolution, Medicine, and Public Health. 2016 (1): 1–16. doi:10.1093/emph/eov033. PMC 4703052. PMID 26739325.
  13. ^ van der Most PJ, de Jong B, Parmentier HK, Verhulst S (February 2011). "Trade‐off between growth and immune function: a meta‐analysis of selection experiments". Functional Ecology. 25 (1): 74–80. doi:10.1111/j.1365-2435.2010.01800.x. ISSN 0269-8463.
  14. ^ Urlacher SS, Ellison PT, Sugiyama LS, Pontzer H, Eick G, Liebert MA, et al. (April 2018). "Tradeoffs between immune function and childhood growth among Amazonian forager-horticulturalists". Proceedings of the National Academy of Sciences of the United States of America. 115 (17): E3914–E3921. doi:10.1073/pnas.1717522115. PMC 5924892. PMID 29632170.
  15. ^ Brace AJ, Lajeunesse MJ, Ardia DR, Hawley DM, Adelman JS, Buchanan KL, et al. (June 2017). "Costs of immune responses are related to host body size and lifespan". Journal of Experimental Zoology Part A: Ecological and Integrative Physiology. 327 (5): 254–261. doi:10.1002/jez.2084. PMC 5786166. PMID 29356459.
  16. ^ a b French SS, Moore MC, Demas GE (September 2009). "Ecological immunology: The organism in context". Integrative and Comparative Biology. 49 (3): 246–253. doi:10.1093/icb/icp032. PMID 21665817.
  17. ^ Demas GE (March 2004). "The energetics of immunity: a neuroendocrine link between energy balance and immune function". Hormones and Behavior. 45 (3): 173–180. doi:10.1016/j.yhbeh.2003.11.002. PMID 15047012. S2CID 14365109.
  18. ^ a b Lutton B, Callard I (December 2006). "Evolution of reproductive-immune interactions". Integrative and Comparative Biology. 46 (6): 1060–1071. doi:10.1093/icb/icl050. PMID 21672808.
  19. ^ Hicks O, Green JA, Daunt F, Cunningham EJ, Newell M, Butler A, Burthe SJ (August 2019). "Sublethal effects of natural parasitism act through maternal, but not paternal, reproductive success in a wild population". Ecology. 100 (8): e02772. doi:10.1002/ecy.2772. PMC 6851849. PMID 31165474.
  20. ^ Smyth KN, Drea CM (2016-01-01). "Patterns of parasitism in the cooperatively breeding meerkat: a cost of dominance for females". Behavioral Ecology. 27 (1): 148–157. doi:10.1093/beheco/arv132. ISSN 1045-2249.
  21. ^ Habig B, Doellman MM, Woods K, Olansen J, Archie EA (February 2018). "Social status and parasitism in male and female vertebrates: a meta-analysis". Scientific Reports. 8 (1): 3629. Bibcode:2018NatSR...8.3629H. doi:10.1038/s41598-018-21994-7. PMC 5827031. PMID 29483573.
  22. ^ a b Albery GF, Watt KA, Keith R, Morris S, Morris A, Kenyon F, et al. (January 2020). Gremillet D (ed.). "Reproduction has different costs for immunity and parasitism in a wild mammal". Functional Ecology. 34 (1): 229–239. doi:10.1111/1365-2435.13475. hdl:20.500.11820/95179f63-7c86-4fe3-8e66-5001f6632c91. ISSN 0269-8463. S2CID 209586422.
  23. ^ Abrams ET, Miller EM (2011). "The roles of the immune system in women's reproduction: evolutionary constraints and life history trade-offs". American Journal of Physical Anthropology. 146 (Suppl 53): 134–154. doi:10.1002/ajpa.21621. PMID 22101690.
  24. ^ a b Bribiescas RG (2001). "Reproductive ecology and life history of the human male". American Journal of Physical Anthropology. 116 (Suppl 33): 148–176. doi:10.1002/ajpa.10025. PMID 11786994.
  25. ^ a b c d Muehlenbein MP (March 2006). "Adaptive variation in testosterone levels in response to immune activation: empirical and theoretical perspectives". Social Biology. 53 (1–2): 13–23. doi:10.1080/19485565.2006.9989113. PMID 21516947. S2CID 25730983.
  26. ^ Spratt DI, Cox P, Orav J, Moloney J, Bigos T (June 1993). "Reproductive axis suppression in acute illness is related to disease severity". The Journal of Clinical Endocrinology and Metabolism. 76 (6): 1548–1554. doi:10.1210/jcem.76.6.8501163. PMID 8501163.
  27. ^ Poretsky L, Can S, Zumoff B (July 1995). "Testicular dysfunction in human immunodeficiency virus-infected men". Metabolism. 44 (7): 946–953. doi:10.1016/0026-0495(95)90250-3. PMID 7616856.
  28. ^ Padgett DA, Glaser R (March 2003). "How stress influences the immune response". Trends in Immunology. 24 (8): 444–448. doi:10.1016/S1471-4906(03)00173-X. PMID 12909458.
  29. ^ a b c Webster Marketon JI, Glaser R (2008-01-01). "Stress hormones and immune function". Cellular Immunology. Neuroendocrine Regulation of Immune Function. 252 (1–2): 16–26. doi:10.1016/j.cellimm.2007.09.006. PMID 18279846.
  30. ^ Padgett DA, Sheridan JF, Dorne J, Berntson GG, Candelora J, Glaser R (June 1998). "Social stress and the reactivation of latent herpes simplex virus type 1". Proceedings of the National Academy of Sciences of the United States of America. 95 (12): 7231–7235. Bibcode:1998PNAS...95.7231P. doi:10.1073/pnas.95.12.7231. PMC 22787. PMID 9618568.
  31. ^ Griebel P, Hill K, Stookey J (December 2014). "How stress alters immune responses during respiratory infection". Animal Health Research Reviews. 15 (2): 161–165. doi:10.1017/s1466252314000280. PMID 25497501. S2CID 206331639.
  32. ^ Cohen F, Kemeny ME, Kearney KA, Zegans LS, Neuhaus JM, Conant MA (November 1999). "Persistent stress as a predictor of genital herpes recurrence". Archives of Internal Medicine. 159 (20): 2430–2436. doi:10.1001/archinte.159.20.2430. PMID 10665891.
  33. ^ Coskun O, Sener K, Kilic S, Erdem H, Yaman H, Besirbellioglu AB, et al. (March 2010). "Stress-related Epstein-Barr virus reactivation". Clinical and Experimental Medicine. 10 (1): 15–20. doi:10.1007/s10238-009-0063-z. PMID 19779966. S2CID 25629238.
  34. ^ Beani L, Mariotti Lippi M, Mulinacci N, Manfredini F, Cecchi L, Giuliani C, et al. (December 2020). "Altered feeding behavior and immune competence in paper wasps: A case of parasite manipulation?". PLOS ONE. 15 (12): e0242486. Bibcode:2020PLoSO..1542486B. doi:10.1371/journal.pone.0242486. PMC 7743958. PMID 33326432.
  35. ^ Koella JC, Sørensen FL, Anderson RA (May 1998). "The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae". Proceedings. Biological Sciences. 265 (1398): 763–768. doi:10.1098/rspb.1998.0358. PMC 1689045. PMID 9628035.
  36. ^ Sargent LW, Baldridge AK, Vega-Ross M, Towle KM, Lodge DM (July 2014). "A trematode parasite alters growth, feeding behavior, and demographic success of invasive rusty crayfish (Orconectes rusticus)". Oecologia. 175 (3): 947–958. Bibcode:2014Oecol.175..947S. doi:10.1007/s00442-014-2939-1. PMID 24710690. S2CID 8060013.
  37. ^ Lafferty KD, Morris AK (July 1996). "Altered Behavior of Parasitized Killifish Increases Susceptibility to Predation by Bird Final Hosts". Ecology. 77 (5): 1390–1397. doi:10.2307/2265536. JSTOR 2265536.
  38. ^ Stafford-Banks CA, Yang LH, McMunn MS, Ullman DE (November 2014). "Virus infection alters the predatory behavior of an omnivorous vector". Oikos. 123 (11): 1384–1390. doi:10.1111/oik.01148.
  39. ^ a b Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (April 2006). "Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar". Proceedings. Biological Sciences. 273 (1588): 823–829. doi:10.1098/rspb.2005.3385. PMC 1560230. PMID 16618675.
  40. ^ a b c Bernardo MA, Singer MS (August 2017). "Parasite-altered feeding behavior in insects: integrating functional and mechanistic research frontiers". The Journal of Experimental Biology. 220 (Pt 16): 2848–2857. doi:10.1242/jeb.143800. PMID 28814608. S2CID 41579370.
  41. ^ a b Simone-Finstrom MD, Spivak M (March 2012). Marion-Poll F (ed.). "Increased resin collection after parasite challenge: a case of self-medication in honey bees?". PLOS ONE. 7 (3): e34601. Bibcode:2012PLoSO...734601S. doi:10.1371/journal.pone.0034601. PMC 3315539. PMID 22479650.
  42. ^ Wrangham RW (1995). "Relationship of chimpanzee leaf-swallowing to a tapeworm infection". American Journal of Primatology. 37 (4): 297–303. doi:10.1002/ajp.1350370404. PMID 31936954. S2CID 85326514.
  43. ^ Huffman MA, Spiezio C, Sgaravatti A, Leca JB (November 2010). "Leaf swallowing behavior in chimpanzees (Pan troglodytes): biased learning and the emergence of group level cultural differences". Animal Cognition. 13 (6): 871–880. doi:10.1007/s10071-010-0335-8. PMID 20602132. S2CID 13296284.
  44. ^ Hutchings MR, Athanasiadou S, Kyriazakis I, Gordon IJ (May 2003). "Can animals use foraging behaviour to combat parasites?". The Proceedings of the Nutrition Society. 62 (2): 361–370. doi:10.1079/PNS2003243. PMID 14506883. S2CID 26061375.
  45. ^ Manson JS, Otterstatter MC, Thomson JD (January 2010). "Consumption of a nectar alkaloid reduces pathogen load in bumble bees". Oecologia. 162 (1): 81–89. Bibcode:2010Oecol.162...81M. doi:10.1007/s00442-009-1431-9. PMID 19711104. S2CID 25322910.
  46. ^ Cremer S, Armitage SA, Schmid-Hempel P (August 2007). "Social immunity". Current Biology. 17 (16): R693–R702. doi:10.1016/j.cub.2007.06.008. PMID 17714663. S2CID 7052797.
  47. ^ Lochmiller RL, Deerenberg C (January 2000). "Trade-offs in evolutionary immunology: just what is the cost of immunity?". Oikos. 88 (1): 87–98. doi:10.1034/j.1600-0706.2000.880110.x. ISSN 0030-1299.
  48. ^ a b c d e Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT (January 2009). "Introduction. Ecological immunology". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 364 (1513): 3–14. doi:10.1098/rstb.2008.0249. PMC 2666701. PMID 18926970.
  49. ^ Kraaijeveld AR, Godfray HC (September 1997). "Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster". Nature. 389 (6648): 278–280. Bibcode:1997Natur.389..278K. doi:10.1038/38483. PMID 9305840. S2CID 205026562.
  50. ^ French SS, Dearing MD, Demas GE (October 2011). "Leptin as a physiological mediator of energetic trade-offs in ecoimmunology: implications for disease". Integrative and Comparative Biology. 51 (4): 505–513. doi:10.1093/icb/icr019. PMC 6281385. PMID 21940777.
  51. ^ Moeller AH, Li Y, Mpoudi Ngole E, Ahuka-Mundeke S, Lonsdorf EV, Pusey AE, et al. (November 2014). "Rapid changes in the gut microbiome during human evolution". Proceedings of the National Academy of Sciences of the United States of America. 111 (46): 16431–16435. Bibcode:2014PNAS..11116431M. doi:10.1073/pnas.1419136111. PMC 4246287. PMID 25368157.
  52. ^ a b Amato KR, Jeyakumar T, Poinar H, Gros P (October 2019). "Shifting Climates, Foods, and Diseases: The Human Microbiome through Evolution". BioEssays. 41 (10): e1900034. doi:10.1002/bies.201900034. PMID 31524305. S2CID 202581640.
  53. ^ Hu GZ, Yang SJ, Hu WX, Wen Z, He D, Zeng LF, et al. (January 2016). "Effect of cold stress on immunity in rats". Experimental and Therapeutic Medicine. 11 (1): 33–42. doi:10.3892/etm.2015.2854. PMC 4726882. PMID 26889214.
  54. ^ a b Randolph HE, Fiege JK, Thielen BK, Mickelson CK, Shiratori M, Barroso-Batista J, et al. (November 2021). "Genetic ancestry effects on the response to viral infection are pervasive but cell type specific". Science. 374 (6571): 1127–1133. Bibcode:2021Sci...374.1127R. doi:10.1126/science.abg0928. PMC 8957271. PMID 34822289.
  55. ^ a b Fumagalli M, Sironi M, Pozzoli U, Ferrer-Admetlla A, Ferrer-Admettla A, Pattini L, Nielsen R (November 2011). "Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution". PLOS Genetics. 7 (11): e1002355. doi:10.1371/journal.pgen.1002355. PMC 3207877. PMID 22072984.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  56. ^ Enard D, Petrov DA (October 2018). "Evidence that RNA Viruses Drove Adaptive Introgression between Neanderthals and Modern Humans". Cell. 175 (2): 360–371.e13. doi:10.1016/j.cell.2018.08.034. PMC 6176737. PMID 30290142.
  57. ^ Pedersen AB, Babayan SA (March 2011). "Wild immunology". Molecular Ecology. 20 (5): 872–880. doi:10.1111/j.1365-294X.2010.04938.x. PMID 21324009. S2CID 9692150.
  58. ^ a b c Downs CJ, Adelman JS, Demas GE (September 2014). "Mechanisms and methods in ecoimmunology: integrating within-organism and between-organism processes". Integrative and Comparative Biology. 54 (3): 340–352. doi:10.1093/icb/icu082. PMID 24944113.
  59. ^ Best A, White A, Boots M (June 2009). "The implications of coevolutionary dynamics to host-parasite interactions". The American Naturalist. 173 (6): 779–791. doi:10.1086/598494. PMID 19374557. S2CID 24108279.
  60. ^ Luciani F, Alizon S (November 2009). "The evolutionary dynamics of a rapidly mutating virus within and between hosts: the case of hepatitis C virus". PLOS Computational Biology. 5 (11): e1000565. Bibcode:2009PLSCB...5E0565L. doi:10.1371/journal.pcbi.1000565. PMC 2768904. PMID 19911046.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  61. ^ Martens E, Demain AL (May 2017). "The antibiotic resistance crisis, with a focus on the United States". The Journal of Antibiotics. 70 (5): 520–526. doi:10.1038/ja.2017.30. PMID 28246379. S2CID 24758375.
  62. ^ Vale PF, Fenton A, Brown SP (January 2014). "Limiting damage during infection: lessons from infection tolerance for novel therapeutics". PLOS Biology. 12 (1): e1001769. doi:10.1371/journal.pbio.1001769. PMC 3897360. PMID 24465177.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  63. ^ Vale PF, McNally L, Doeschl-Wilson A, King KC, Popat R, Domingo-Sananes MR, et al. (2016). "Beyond killing: Can we find new ways to manage infection?". Evolution, Medicine, and Public Health. 2016 (1): 148–157. doi:10.1093/emph/eow012. PMC 4834974. PMID 27016341.
  64. ^ Totsika M (March 2017). "Disarming pathogens: benefits and challenges of antimicrobials that target bacterial virulence instead of growth and viability". Future Medicinal Chemistry. 9 (3): 267–269. doi:10.4155/fmc-2016-0227. PMID 28207349.
Retrieved from "https://en.wikipedia.org/w/index.php?title=Ecoimmunology&oldid=1098108791"