Mammalian endothermy optimally restricts fungi and metabolic costs

Aviv Bergman, Arturo Casadevall

Research output: Contribution to journalArticle

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. IMPORTANCE Mammals are characterized by both maintaining and closely regulating high body temperatures, processes that are known as endothermy and homeothermy, respectively. The mammalian lifestyle is energy intensive and costly. The evolutionary mechanisms responsible for the emergence and success of these mammalian characteristics are not understood. This work suggests that high mammalian temperatures represent optima in the tradeoff between metabolic costs and the increased fitness that comes with resistance to fungal diseases.

Original languageEnglish (US)
Article numbere00212-10
JournalmBio
Volume1
Issue number5
DOIs
StatePublished - Nov 2010
Externally publishedYes

Fingerprint

Mycoses
Fungi
Body Temperature
Costs and Cost Analysis
Mammals
Temperature
Hot Temperature
Communicable Diseases
Vertebrates
Life Style
Growth

ASJC Scopus subject areas

  • Microbiology
  • Virology

Cite this

Mammalian endothermy optimally restricts fungi and metabolic costs. / Bergman, Aviv; Casadevall, Arturo.

In: mBio, Vol. 1, No. 5, e00212-10, 11.2010.

Research output: Contribution to journalArticle

@article{49dff8a7927a489bbcd8fab4b4260ebf,
title = "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. IMPORTANCE Mammals are characterized by both maintaining and closely regulating high body temperatures, processes that are known as endothermy and homeothermy, respectively. The mammalian lifestyle is energy intensive and costly. The evolutionary mechanisms responsible for the emergence and success of these mammalian characteristics are not understood. This work suggests that high mammalian temperatures represent optima in the tradeoff between metabolic costs and the increased fitness that comes with resistance to fungal diseases.",
author = "Aviv Bergman and Arturo Casadevall",
year = "2010",
month = "11",
doi = "10.1128/mBio.00212-10",
language = "English (US)",
volume = "1",
journal = "mBio",
issn = "2161-2129",
publisher = "American Society for Microbiology",
number = "5",

}

TY - JOUR

T1 - Mammalian endothermy optimally restricts fungi and metabolic costs

AU - Bergman, Aviv

AU - Casadevall, Arturo

PY - 2010/11

Y1 - 2010/11

N2 - 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. IMPORTANCE Mammals are characterized by both maintaining and closely regulating high body temperatures, processes that are known as endothermy and homeothermy, respectively. The mammalian lifestyle is energy intensive and costly. The evolutionary mechanisms responsible for the emergence and success of these mammalian characteristics are not understood. This work suggests that high mammalian temperatures represent optima in the tradeoff between metabolic costs and the increased fitness that comes with resistance to fungal diseases.

AB - 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. IMPORTANCE Mammals are characterized by both maintaining and closely regulating high body temperatures, processes that are known as endothermy and homeothermy, respectively. The mammalian lifestyle is energy intensive and costly. The evolutionary mechanisms responsible for the emergence and success of these mammalian characteristics are not understood. This work suggests that high mammalian temperatures represent optima in the tradeoff between metabolic costs and the increased fitness that comes with resistance to fungal diseases.

UR - http://www.scopus.com/inward/record.url?scp=79952161654&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79952161654&partnerID=8YFLogxK

U2 - 10.1128/mBio.00212-10

DO - 10.1128/mBio.00212-10

M3 - Article

C2 - 21060737

AN - SCOPUS:79952161654

VL - 1

JO - mBio

JF - mBio

SN - 2161-2129

IS - 5

M1 - e00212-10

ER -