Mammalian endothermy optimally restricts fungi and metabolic costs
- PMID: 21060737
- PMCID: PMC2975364
- DOI: 10.1128/mBio.00212-10
Mammalian endothermy optimally restricts fungi and metabolic costs
Abstract
Endothermy and homeothermy are mammalian characteristics whose evolutionary origins are poorly understood. Given that fungal species rapidly lose their capacity for growth above ambient temperatures, we have proposed that mammalian endothermy enhances fitness by creating exclusionary thermal zones that protect against fungal disease. According to this view, the relative paucity of invasive fungal diseases in immunologically intact mammals relative to other infectious diseases would reflect an inability of most fungal species to establish themselves in a mammalian host. In this study, that hypothesis was tested by modeling the fitness increase with temperature versus its metabolic costs. We analyzed the tradeoff involved between the costs of the excess metabolic rates required to maintain a body temperature and the benefit gained by creating a thermal exclusion zone that protects against environmental microbes such as fungi. The result yields an optimum at 36.7°C, which closely approximates mammalian body temperatures. This calculation is consistent with and supportive of the notion that an intrinsic thermally based resistance against fungal diseases could have contributed to the success of mammals in the Tertiary relative to that of other vertebrates.
Figures
Similar articles
-
Vertebrate endothermy restricts most fungi as potential pathogens.J Infect Dis. 2009 Nov 15;200(10):1623-6. doi: 10.1086/644642. J Infect Dis. 2009. PMID: 19827944
-
Fungal virulence, vertebrate endothermy, and dinosaur extinction: is there a connection?Fungal Genet Biol. 2005 Feb;42(2):98-106. doi: 10.1016/j.fgb.2004.11.008. Epub 2005 Jan 5. Fungal Genet Biol. 2005. PMID: 15670708 Review.
-
Two fundamentals of mammalian defense in fungal infections: endothermy and innate antifungal immunity.Pol J Vet Sci. 2014;17(3):555-67. doi: 10.2478/pjvs-2014-0084. Pol J Vet Sci. 2014. PMID: 25286672 Review.
-
Global warming will bring new fungal diseases for mammals.mBio. 2010 May 18;1(1):e00061-10. doi: 10.1128/mBio.00061-10. mBio. 2010. PMID: 20689745 Free PMC article.
-
Seasonal reproductive endothermy in tegu lizards.Sci Adv. 2016 Jan 22;2(1):e1500951. doi: 10.1126/sciadv.1500951. eCollection 2016 Jan. Sci Adv. 2016. PMID: 26844295 Free PMC article.
Cited by
-
Response and regulatory mechanisms of heat resistance in pathogenic fungi.Appl Microbiol Biotechnol. 2022 Sep;106(17):5415-5431. doi: 10.1007/s00253-022-12119-2. Epub 2022 Aug 9. Appl Microbiol Biotechnol. 2022. PMID: 35941254 Free PMC article. Review.
-
Basic principles of the virulence of Cryptococcus.Virulence. 2019 Dec;10(1):490-501. doi: 10.1080/21505594.2019.1614383. Virulence. 2019. PMID: 31119976 Free PMC article. Review.
-
Benefits and Costs of Animal Virulence for Microbes.mBio. 2019 Jun 4;10(3):e00863-19. doi: 10.1128/mBio.00863-19. mBio. 2019. PMID: 31164465 Free PMC article. Review.
-
Thermal control of microbial development and virulence: molecular mechanisms of microbial temperature sensing.mBio. 2012 Oct 2;3(5):e00238-12. doi: 10.1128/mBio.00238-12. Print 2012. mBio. 2012. PMID: 23033469 Free PMC article. Review.
-
Love in the time of climate change: A review of sexual reproduction in the order Onygenales.Fungal Genet Biol. 2023 Jun;167:103797. doi: 10.1016/j.fgb.2023.103797. Epub 2023 Apr 24. Fungal Genet Biol. 2023. PMID: 37100376 Free PMC article. Review.
References
-
- Kemp T. S. 2008. The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure. Zool. J. Linn. Soc. 147:473–488
-
- Ruben J. 1995. The evolution of endothermy in mammals and birds: from physiology to fossils. Annu. Rev. Physiol. 57:69–95 - PubMed
-
- Robert V. A., Casadevall A. 2009. Vertebrate endothermy restricts most fungi as potential pathogens. J. Infect. Dis. 200:1623–1626 - PubMed
-
- Casadevall A. 2005. Fungal virulence, vertebrate endothermy, and dinosaur extinction: is there a connection? Fungal Genet. Biol. 42:98–106 - PubMed
-
- Gillooly J. F., Brown J. H., West G. B., Savage V. M., Charnov E. L. 2001. Effects of size and temperature on metabolic rate. Science 293:2248–2251 - PubMed
Publication types
MeSH terms
Grants and funding
- R01 AI033142/AI/NIAID NIH HHS/United States
- AI33142-11/AI/NIAID NIH HHS/United States
- R01 AI033774/AI/NIAID NIH HHS/United States
- R01 AG028872/AG/NIA NIH HHS/United States
- HL59842-07/HL/NHLBI NIH HHS/United States
- AI52733-02/AI/NIAID NIH HHS/United States
- R01 AI052733/AI/NIAID NIH HHS/United States
- P01 AG027734/AG/NIA NIH HHS/United States
- AI33774-11/AI/NIAID NIH HHS/United States
- R01 HL059842/HL/NHLBI NIH HHS/United States
- 5R01AG028872-04/AG/NIA NIH HHS/United States
- U54-AI057158-LIPKIN/AI/NIAID NIH HHS/United States
- U54 AI057158/AI/NIAID NIH HHS/United States
- 5P01AG027734-04/AG/NIA NIH HHS/United States
- R37 AI033142/AI/NIAID NIH HHS/United States
LinkOut - more resources
Full Text Sources
Medical