TY - JOUR
T1 - The heat dissipation limit theory and evolution of life histories in endotherms-time to dispose of the disposable soma theory?
AU - Speakman, John R.
AU - Król, Elzbieta
N1 - We thank James Harper and Anne Bronikowski for the invitation to speak at the symposium, which stimulated this review. We are grateful to many past and present students, postdoctoral fellows, and colleagues for their direct and indirect inputs into the ideas in this article; Don Thomas, Henk Visser, Steve Austad, Simon Verhulst, Serge Daan, Murray Humphries, Colin Selman, Kim Hammond, Shelly Buffenstein, Tony Hulbert, Martin Brand, Zhijun Zhao, Dehua Wang, and Craig White all made useful contributions. We also thank João Pedro de Magalhães, Harold Heatwole, and an anonymous reviewer for their extensive and invaluable comments on earlier drafts of the article.
PY - 2010/5/21
Y1 - 2010/5/21
N2 - Synopsis A major factor influencing life-history strategies of endotherms is body size. Larger endotherms live longer, develop more slowly, breed later and less frequently, and have fewer offspring per attempt at breeding. The classical evolutionary explanation for this pattern is that smaller animals experience greater extrinsic mortality, which favors early reproduction at high intensity. This leads to a short lifespan and early senescence by three suggested mechanisms. First, detrimental late-acting mutations cannot be removed because of the low force of selection upon older animals (mutation accumulation). Second, genes that promote early reproduction will be favored in small animals, even if they have later detrimental effects (antagonistic pleiotropy). Third, small animals may be forced to reduce their investment in longevity assurance mechanisms (LAMs) in favor of investment in reproduction (the disposable soma theory, DST). The DST hinges on three premises: that LAMs exist, that such LAMs are energetically expensive and that the supply of energy is limited. By contrast, the heat dissipation limit (HDL) theory provides a different conceptual perspective on the evolution of life histories in relation to body size. We suggest that rather than being limited, energy supplies in the environment are often unlimited, particularly when animals are breeding, and that animals are instead constrained by their maximum capacity to dissipate body heat, generated as a by-product of their metabolism. Because heat loss is fundamentally a surface-based phenomenon, the low surface-to-volume ratio of larger animals generates significant problems for dissipating the body heat associated with reproductive effort, which then limits their current reproductive investment. We suggest that this is the primary reason why fecundity declines as animal size increases. Because large animals are constrained by their capacity for heat dissipation, they have low reproductive rates. Consequently, only those large animals living in habitats with low extrinsic mortality could survive leading to the familiar patterns of life-history trade-offs and their links to extrinsic mortality rates. The HDL theory provides a novel mechanism underpinning the evolution of life history and ageing in endotherms, and makes a number of testable predictions that directly contrast with the predictions arising from the DST.
AB - Synopsis A major factor influencing life-history strategies of endotherms is body size. Larger endotherms live longer, develop more slowly, breed later and less frequently, and have fewer offspring per attempt at breeding. The classical evolutionary explanation for this pattern is that smaller animals experience greater extrinsic mortality, which favors early reproduction at high intensity. This leads to a short lifespan and early senescence by three suggested mechanisms. First, detrimental late-acting mutations cannot be removed because of the low force of selection upon older animals (mutation accumulation). Second, genes that promote early reproduction will be favored in small animals, even if they have later detrimental effects (antagonistic pleiotropy). Third, small animals may be forced to reduce their investment in longevity assurance mechanisms (LAMs) in favor of investment in reproduction (the disposable soma theory, DST). The DST hinges on three premises: that LAMs exist, that such LAMs are energetically expensive and that the supply of energy is limited. By contrast, the heat dissipation limit (HDL) theory provides a different conceptual perspective on the evolution of life histories in relation to body size. We suggest that rather than being limited, energy supplies in the environment are often unlimited, particularly when animals are breeding, and that animals are instead constrained by their maximum capacity to dissipate body heat, generated as a by-product of their metabolism. Because heat loss is fundamentally a surface-based phenomenon, the low surface-to-volume ratio of larger animals generates significant problems for dissipating the body heat associated with reproductive effort, which then limits their current reproductive investment. We suggest that this is the primary reason why fecundity declines as animal size increases. Because large animals are constrained by their capacity for heat dissipation, they have low reproductive rates. Consequently, only those large animals living in habitats with low extrinsic mortality could survive leading to the familiar patterns of life-history trade-offs and their links to extrinsic mortality rates. The HDL theory provides a novel mechanism underpinning the evolution of life history and ageing in endotherms, and makes a number of testable predictions that directly contrast with the predictions arising from the DST.
UR - http://www.scopus.com/inward/record.url?scp=78651294960&partnerID=8YFLogxK
U2 - 10.1093/icb/icq049
DO - 10.1093/icb/icq049
M3 - Article
C2 - 21558242
AN - SCOPUS:78651294960
SN - 1540-7063
VL - 50
SP - 793
EP - 807
JO - Integrative and Comparative Biology
JF - Integrative and Comparative Biology
IS - 5
ER -