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Climatic Adaptation and the Evolution of Basal and Maximum Rates of Metabolism in Rodents

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Climatic Adaptation and the Evolution of Basal and Maximum Rates of Metabolism in Rodents Evolution, 58(6), 2004, pp. 1361±1374 CLIMATIC ADAPTATION AND THE EVOLUTION OF BASAL AND MAXIMUM RATES OF METABOLISM IN RODENTS ENRICO L. REZENDE,1,2 FRANCISCO BOZINOVIC,3 AND THEODORE GARLAND,JR.1,4 1Department of Biology, University of California, Riverside, California 92521 2E-mail: [email protected] 3Center for Advanced Studies in Ecology and Biodiversity and Departamento de EcologõÂa, Facultad de Ciencias BioloÂgicas, Ponti®cia Universidad CatoÂlica de Chile, Santiago 6513677, Chile E-mail: [email protected] 4E-mail: [email protected] Abstract. Metabolic rate is a key aspect of organismal biology and the identi®cation of selective factors that have led to species differences is a major goal of evolutionary physiology. We tested whether environmental characteristics and/or diet were signi®cant predictors of interspeci®c variation in rodent metabolic rates. Mass-speci®c basal metabolic rates (BMR) and maximum metabolic rates (MMR, measured during cold exposure in a He-O2 atmosphere) were compiled from the literature. Maximum (Tmax) and minimum (Tmin) annual mean temperatures, latitude, altitude, and precipitation were obtained from ®eld stations close to the capture sites reported for each population (N 5 57). Diet and all continuous-valued traits showed statistically signi®cant phylogenetic signal, with the exception of mass- corrected MMR and altitude. Therefore, results of phylogenetic analyses are emphasized. Body mass was not correlated with absolute latitude, but was positively correlated with precipitation in analyses with phylogenetically independent contrasts. Conventional multiple regressions that included body mass indicated that Tmax (best), Tmin, latitude, and diet were signi®cant additional predictors of BMR. However, phylogenetic analyses indicated that latitude was the only signi®cant predictor of mass-adjusted BMR (positive partial regression coef®cient, one-tailed P 5 0.0465). Conventional analyses indicated that Tmax, Tmin (best), and altitude explained signi®cant amounts of the variation in mass-adjusted MMR. With body mass and Tmin in the model, no additional variables were signi®cant predictors. Phylogenetic contrasts yielded similar results. Both conventional and phylogenetic analyses indicated a highly sig- ni®cant positive correlation between residual BMR and MMR (as has also been reported for birds), which is consistent with a key assumption of the aerobic capacity model for the evolution of vertebrate energetics (assuming that MMR and exercise-induced maximal oxygen consumption are positively functionally related). Our results support the hy- pothesis that variation in environmental factors leads to variation in the selective regime for metabolic rates of rodents. However, the causes of a positive association between BMR and latitude remain obscure. Moreover, an important area for future research will be experiments in all taxa are raised under common conditions to allow de®nitive tests of climatic adaptation in endotherm metabolic rates and to elucidate the extent of adaptive phenotypic plasticity. Key words. Bergmann's rule, body size, comparative method, diet, endothermy, energetics, temperature. Received August 29, 2003. Accepted February 8, 2004. Identi®cation of the selective factors that have led to in- lations (i.e., grade shifts) have been identi®ed by conven- terspeci®c diversi®cation in metabolic rates has been a major tional analysis of covariance (ANCOVA), and clade-speci®c goal of ecological and evolutionary physiology (Garland and allometric equations have been developed (e.g., MacMillen Carter 1994; Spicer and Gaston 1999; Walters and Reich and Nelson 1969; Dawson and Hulbert 1970; Hayssen and 2000; McNab 2002). The most common approach is to cor- Lacy 1985; McNab 1988, 2002; MacMillen and Garland relate species or population differences in metabolic rate with 1989; Koteja and Weiner 1993). However, to our knowledge variation in various biotic (e.g., diet) or abiotic (e.g., altitude, the clade differences have not been demonstrated with phy- latitude, ambient temperature) factors. Mammals have been logenetically based statistical analyses (e.g., see Garland et the most common subjects of such studies, and signi®cant al. 1993; Cruz-Neto et al. 2001; with respect to avian met- correlations are generally taken as evidence of metabolic ad- abolic rates, see Garland and Ives 2000; Rezende et al. 2002). aptation in the genetic, evolutionary sense, although a variety Aside from possible clade differences, several studies have of caveats apply (see Discussion). attempted to explain the residual variation in BMR (i.e., after Basal metabolic rate (BMR) is the usual estimate of the correlations with body size have been controlled statistically) metabolic ¯oor in mammals. It is generally measured as the by associations with various biotic or abiotic factors (for rate of oxygen uptake during the inactive part of the 24-h reviews, see Leonard et al. 2002; McNab 2002). Interspeci®c cycle, of a postabsorptive, nonactive, reproductively adult comparisons of mammalian BMR have reported a signi®cant individual (but not in reproductive condition), at an air tem- association with diet using conventional statistics (McNab perature within its thermal neutral zone (McNab 1988). Since 1992, 2002, 2003), but not with phylogenetically based meth- Kleiber (1932), the main factor identi®ed as explaining in- ods (Degen et al. 1998; Speakman 2000; Cruz-Neto et al. terspeci®c variation in BMR has been variation in body mass. 2001; Genoud 2002). Environmental productivity (as an in- Given a large enough body-size range, larger-bodied species dex of food availability) has also been suggested to in¯uence have lower mass-speci®c BMR, although the precise allo- BMR (Hayes 1989; Mueller and Diamond 2001; White 2003), metric scaling exponent is controversial for a variety of rea- and a signi®cant positive correlation between mass-indepen- sons (e.g., Symonds and Elgar 2002; White and Seymour dent BMR and net primary productivity was reported for a 2003). Clades differences in the elevations of allometric re- comparison of ®ve species of Peromyscus mice (Mueller and 1361 q 2004 The Society for the Study of Evolution. All rights reserved. 1362 ENRICO L. REZENDE ET AL. Diamond 2001, phylogenetic analysis). Comparative studies have similarly restricted themselves to particular lineages of small mammals have also reported signi®cant associations (e.g., MacMillen and Garland 1989, Peromyscus; Hinds and between habitat aridity and BMRÐthat is, species from (hot) Rice-Warner 1992, rodents; Degen et al. 1998, rodents; Sparti deserts have lower BMRs than their counterparts from mesic 1992, shrews; Taylor 1998, shrews; Symonds 1999, Insec- environmentsÐemploying conventional (McNab 1979; Goy- tivora). We discuss our results in the context of geographical al and Gosh 1983; Hulbert et al. 1985) and phylogenetic distribution and the aerobic capacity model of vertebrate en- (Degen et al. 1998) analyses. A signi®cant negative corre- ergetics. In addition, we test whether body mass itself is lation between mean environmental temperatures and mass- associated with environmental variables or diet. This is im- independent BMR has also been reported (MacMillen and portant because the most obvious way that selection can alter Garland 1989, nonphylogenetic; Lovegrove 2003, phyloge- overall energy budgets is through modi®cation of the size of netic). Mass-corrected BMR was also positively associated an organism (Schmidt-Nielsen 1995; Brown and West 2000; with latitude in rodents (MacMillen and Garland 1989; McNab 2002, and references therein). Speakman 2000, both nonphylogenetic; Lovegrove 2003) and birds (Weathers 1979; Ellis 1985, nonphylogenetic), although METHODS effects of temperature were not controlled except in Metabolic and Environmental Data MacMillen and Garland (1989; see Discussion). Maximum metabolic rate (MMR) is typically measured as Because BMR has been extensively studied in mammals the highest rate of oxygen consumption in response to cold (e.g., McNab 1988; Lovegrove 2000), our search focused on challenge (often termed summit metabolism) or forced ex- MMR and was restricted to studies that used cold exposure ercise (VO2max). Although exercise-induced VO2max can, in in a He-O2 atmosphere to elicit MMR (Rosenmann and Mor- principle, be obtained from terrestrial mammals of virtually rison 1974), to avoid potential problems arising from dif- any size (Seeherman et al. 1981), measurement of cold-in- ferent experimental procedures. We used studies that (1) in- duced MMR is typically only attempted with endotherms cluded both BMR and MMR, measured in the same popu- smaller than about 2 kg (Hinds et al. 1993; but see Fournier lation and, when possible, in the same individuals; (2) in- and Thomas 1999), especially when the He-O2 technique is volved animals captured in the ®eld, or were maintained for used (see Methods). To our knowledge, only two comparative only a few generations in the laboratory (Baiomys taylori, studies of residual variation in MMR have been published one or two generations in the lab, M. Rosenmann, pers. (Bozinovic and Rosenmann 1989; Sparti 1992; see also Tay- comm.; Liomys salvini, individuals were maintained 12 lor 1998). months in captivity, Hulbert et al. 1985); and (3) reported One limitation of all of the above-mentioned studies is that original collecting sites. Given these criteria, the following they have tested for biotic or abiotic correlates of a single species were not included in the
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