Received: 23 June 2019 | Revised: 30 December 2019 | Accepted: 7 January 2020 DOI: 10.1111/geb.13069 RESEARCH PAPER No evidence for the ‘rate-of-living’ theory across the tetrapod tree of life Gavin Stark1 | Daniel Pincheira-Donoso2 | Shai Meiri1,3 1School of Zoology, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel Abstract 2School of Biological Sciences, Queen’s Aim: The ‘rate-of-living’ theory predicts that life expectancy is a negative function of University Belfast, Belfast, United Kingdom the rates at which organisms metabolize. According to this theory, factors that accel- 3The Steinhardt Museum of Natural History, Tel Aviv University, Tel Aviv, Israel erate metabolic rates, such as high body temperature and active foraging, lead to organismic ‘wear-out’. This process reduces life span through an accumulation of bio- Correspondence Gavin Stark, School of Zoology, Faculty of chemical errors and the build-up of toxic metabolic by-products. Although the rate- Life Sciences, Tel Aviv University, Tel Aviv, of-living theory is a keystone underlying our understanding of life-history trade-offs, 6997801, Israel. Email: [email protected] its validity has been recently questioned. The rate-of-living theory has never been tested on a global scale in a phylogenetic framework, or across both endotherms and Editor: Richard Field ectotherms. Here, we test several of its fundamental predictions across the tetrapod tree of life. Location: Global. Time period: Present. Major taxa studied: Land vertebrates. Methods: Using a dataset spanning the life span data of 4,100 land vertebrate spe- cies (2,214 endotherms, 1,886 ectotherms), we performed the most comprehensive test to date of the fundamental predictions underlying the rate-of-living theory. We investigated how metabolic rates, and a range of factors generally perceived to be strongly associated with them, relate to longevity. Results: Our findings did not support the predictions of the rate-of-living theory. Basal and field metabolic rates, seasonality, and activity times, as well as reptile body temperatures and foraging ecology, were found to be unrelated to longevity. In con- trast, lower longevity across ectotherm species was associated with high environ- mental temperatures. Main conclusions: We conclude that the rate-of-living theory does not hold true for terrestrial vertebrates, and suggest that life expectancy is driven by selection arising from extrinsic mortality factors. A simple link between metabolic rates, oxidative damage and life span is not supported. Importantly, our findings highlight the poten- tial for rapid warming, resulting from the current increase in global temperatures, to drive accelerated rates of senescence in ectotherms. KEYWORDS basal metabolic rate, body size, body temperature, environmental temperature, field metabolic rate, longevity, the rate-of-living theory Global Ecol Biogeogr. 2020;00:1–28. wileyonlinelibrary.com/journal/geb © 2020 John Wiley & Sons Ltd | 1 2 | STARK ET AL. 1 | INTRODUCTION and a shorter life span in taxa suffering high extrinsic mortality rates (Kirkwood & Austad, 2000). Under the disposable soma theory, The flame that burns twice as bright burns half as long. early reproduction is thought to expose animals to a greater accu- mulation of age-specific mutations with pleiotropic effects (Gavrilov The light that burns twice as bright burns half as long. & Gavrilova, 2002). This has been associated with the 'antagonistic pleiotropy theory', which suggests that some genes encode pheno- The quotes above, ascribed to Lau Tze (Laozi) and from ‘Blade types that offer benefits early on in life, while also encoding other Runner’, respectively, are thought to convey a universal truth: we have traits that are harmful in advanced age (Hamilton, 1966; Kirkwood, a semi-fixed capacity to do things, and we can either get through them 1977; Kirkwood & Austad, 2000; Medawar, 1952; Réale et al., 2010). intensively and quickly – or relaxedly but over a longer time. A funda- Such harmful traits, expressed late in life, will be invisible to selec- mental principle of life history theory predicts that increased energy tion in animals that reproduce young, but will select strongly against expenditure reduces life expectancy (Finkel & Holbrook, 2000; Furness animals that reproduce at older ages (Williams, Day, Fletcher, & & Speakman, 2008; Glazier, 2015; Hulbert, Pamplona, Buffenstein, Rowe, 2006). & Buttemer, 2007; Magalhães, Costa, & Church, 2007; Pearl, 1928; The rate-of-living theory has been studied in insects, fish, Rubner, 1908; Van Voorhies, Khazaeli, & Curtsinger, 2003). The mech- birds and mammals (Austad & Fischer, 1991; Kelemen, Cao, Cao, anistic explanation for this relationship stems from the assumption Davidowitz, & Dornhaus, 2019; Lindstedt & Calder, 1976; Liu & that higher metabolic rates increase the production of free radicals Walford, 1975; Herreid, 1964). For example, Healy et al. (2014) and other oxidants produced during aerobic respiration. These, in turn, found that metabolic rate was negatively associated with longev- trigger biomolecular damage that accelerates senescence (Barja, 2002; ity in non-volant endotherms (supporting the rate-of-living theory). Beckman & Ames, 1998; Sohal, 2002). In line with these mechanisms, However, several limitations detract from the evidence supporting multiple studies have suggested that an organism's longevity is an it. For example, some studies have ignored the influence of phylo- inverse function of mass-specific metabolic rates (Atanasov, 2005; genetic non-independence (Austad & Fischer, 1991; Hulbert et al., Kapahi et al., 2010; Ku, Brunk, & Sohal, 1993; Sohal, Svensson, Sohal, 2007; Lindstedt & Calder, 1976). Furthermore, some relatively re- & Brunk, 1989; Wright et al., 2004). This trade-off is commonly re- cent studies (Furness & Speakman, 2008; Glazier, 2015; Magalhães ferred to as the ‘rate-of-living’ theory (Pearl, 1928). According to this et al., 2007; Speakman, 2005) contradict the expectations of the theory, degenerative processes lead to a failure of cellular constitu- theory. For example, bats and birds have higher metabolic rates ents due to the accumulation of biochemical errors and the build-up compared to, similar-sized, non-volant mammals (Brunet-Rossinni & of toxic metabolic by-products (Sohal, 1986). In support of this theory, Austad, 2004; Kleiber, 1947; Réale et al., 2010; Wilkinson & Adams, comparative and experimental studies have shown that the increased 2019). Bats, nonetheless, are exceptionally long-lived (Lagunas- expression of free radicals can shorten life span (Barja & Herrero, Rangel, 2019) and use twice as much energy over their lifetimes as 1998; Melov et al., 2000; Orr & Sohal, 1994; Parkes et al., 1998; Sun do similar sized terrestrial mammals (Healy et al., 2014), indicating & Tower, 1999). there is no fixed amount of energy consumption allocated to an or- Some alternative theories (Hamilton, 1966; Kirkwood, 1977; ganism's life span. Kirkwood & Austad, 2000; Medawar, 1952; Réale et al., 2010) have Magalhães et al. (2007) examined the effect of several factors, been proposed to explain the variations in life span among animals. including metabolic rates, on the longevity of 1,456 vertebrate According to the evolutionary theories of senescence, species that species. Their analyses revealed no relationship between metab- are exposed to low intrinsic (e.g., replication errors and metabolic olism and longevity in eutherians and birds, and a negative link in waste products and oxidation damage by reactive agents) and ex- marsupials. That study, however, was almost entirely restricted to trinsic (such as predation, food shortages or accidents) mortality endotherms (94% of the species examined were mammals or birds) rates will adapt by slowing down their ‘pace of life’ (Scharf et al., and thus could not provide a general explanation for the diversity of 2015). Accordingly, they will expand their reproductive potential by longevity across the vertebrate metabolic range. Other such stud- evolving longer life spans (Healy, Ezard, Jones, Salguero-Gómez, & ies (Austad & Fischer, 1991; Furness & Speakman, 2008; Healy et Buckley, 2019; De Magalhães et al., 2007). In contrast, animals that al., 2014; Herreid, 1964; Hulbert et al., 2007; Ku et al., 1993) have are more likely to die due to extrinsic factors, rather than through also focused almost exclusively on birds and mammals. Although se- senescence, benefit from investing in early reproduction at the lection from environmental factors (e.g., ambient temperature) may expense of investment in long-term maintenance (Hamilton, 1966; differ dramatically between endotherms and ectotherms, only a few Kirkwood, 1977; Kirkwood & Austad, 2000; Medawar, 1952). comparative studies (Scharf et al., 2015; Stark & Meiri, 2018) have Life span represents trade-offs between reproduction and main- focused on ectotherm vertebrates, and these have generally ignored tenance (e.g., the ‘disposable soma theory’; Kirkwood, 2017). In metabolic rates. A recent theory (Worm & Tittensor, 2018) suggests taxa facing high extrinsic mortality rates, investing in maintenance that ecological pressures shape evolutionary processes on small is unlikely to pay off if an individual will be preyed upon before it spatial and phylogenetic scales while environmental factors, partic- has a chance to reproduce. According to this theory, this will lead ularly temperature, dominate on larger scales. Environmental effects to selection