The Evolution of High Summit Metabolism and Cold Tolerance in Birds and Its Impact on Present-Day Distributions

Abstract

Summit metabolic rate (M sum , maximum cold-induced metabolic rate) is positively correlated with cold tolerance in birds, suggesting that high M sum is important for residency in cold climates. However, the phylogenetic distribution of high M sum among birds and the impact of its evolution on current distributions are not well understood. Two potential adaptive hypotheses might explain the phylogenetic distribution of high M sum among birds. The cold adaptation hypothesis contends that species wintering in cold climates should have higher M sum than species wintering in warmer climates. The flight adaptation hypothesis suggests that volant birds might be capable of generating high M sum as a byproduct of their muscular capacity for flight; thus, variation in M sum should be associated with capacity for sustained flight, one indicator of which is migration. We collected M sum data from the literature for 44 bird species and conducted both conventional and phylogenetically informed statistical analyses to examine the predictors of M sum variation. Significant phylogenetic signal was present for log body mass, log mass-adjusted M sum , and average temperature in the winter range. In multiple regression models, log body mass, winter temperature, and clade were significant predictors of log M sum . These results are consistent with a role for climate in determining M sum in birds, but also indicate that phylogenetic signal remains even after accounting for associations indicative of adaptation to winter temperature. Migratory strategy was never a significant predictor of log M sum in multiple regressions, a result that is not consistent with the flight adaptation hypothesis. The interplay between physiology and climate can have important consequences for animal distributions. Cold climates require high thermoregulatory energy expenditures for endothermic vertebrates, particularly for small species with high surface area to volume ratios and limited insulatory capacities (Schmidt-Nielsen 1984). Basal (BMR) and maximal cold-induced (=summit metabolism, M sum ) metabolic rates are correlated with climate in mammals, with higher metabolic rates associated with the higher thermoregulatory demands of cold climates (Bozinovic and Rosenmann 1989;Rezende et al. 2004). A similar correlation of BMR with climate also occurs in birds (Weathers 1979), but such correlations of M sum with climate for birds have not been established, primarily because measurements of M sum have mostly been restricted to cold-climate species. The role of winter temperature and the interplay between temperature and metabolism in affecting bird distributions are unclear. Root (1988) found that 1 8 4

Global patterns of seasonal acclimatization in avian resting metabolic rates

“…Msum is generally lower in species from warmer tropical and subtropical environments compared to colder, temperate environments (Swanson and Garland 2009;Wiersma et al 2007a). Our finding that winter residual Msum is significantly higher among temperate-zone species compared to tropical/subtropical species is consistent with this overall picture, as is the corresponding difference in W/S ratios.…”

Are Voluntary Wheel Running and Open-Field Behavior Correlated in Mice? Different Answers from Comparative and Artificial Selection Approaches

“…We tested for any effect of these mutations on wheel running and open-field behavior using RegressionV2.m (Lavin et al 2008). We used a phylogenetic generalized least squares model in which the regression coefficients and the strength of phylogenetic signal in the residuals were estimated (Restricted Maximum Likelihood) simultaneously assuming an Ornstein-Uhlenbeck (OU) evolutionary process along the phylogenetic tree (sensu Swanson and Garland 2009;Gartner et al 2010). The OU model is often used to model stabilizing selection (Garland et al 1993;Hansen 1997;Butler and King 2004).…”

Phylogeny, Ecology, and Heart Position in Snakes

“…Moreover, debates about the importance of ecology versus phylogeny can be addressed statistically by comparison of a range of models in between a star and the original starter tree (e.g., Fig. 1) while simultaneously testing the effects of including ecological (e.g., habitat) and/or phylogenetic (clade membership) variables in alternate models (see also Huey et al 2009;Swanson and Garland 2009). …”

“…It is well known that OLS slopes will underestimate the true scaling relation when the independent variable (in this case, log 10 SVL) contains "measurement error," and if the amount of such error is not known, then the RMA slope often gives a reasonable estimate (Rayner 1985;Warton et al 2006;Ives et al 2007). To obtain the likelihood of the alternative models, we used the Matlab Regressionv2.m program developed by A. R. Ives and T. Garland Jr. (Lavin et al 2008; for examples of applications, see Buchwalter et al 2008;Jeffery et al 2008;Warne and Charnov 2008;Huey et al 2009;Swanson and Garland 2009). …”

“…These AIC comparisons allow for simultaneous consideration of the statistical effects of both phylogeny and ecology on relative heart position. Our overall statistical approach is widely applicable to many questions in comparative biology (see also Huey et al 2009;Swanson and Garland 2009). …”