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Metabolic Scaling in Birds and Mammals: How Taxon Divergence Time, Phylogeny, and Metabolic Rate Affect the Relationship between Scaling Exponents and Intercepts

ABSTRACT:

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This study is based on a large dataset and re-evaluates data on the metabolic rate, providing new insights into the similarities and differences across different groups of birds and mammals. We compared six taxonomic groups of mammals and birds according to their energetic characteristics and the geological time of evolutionary origin. The overall metabolic rate of a taxonomic group increases with the geological time of evolutionary origin. The terrestrial mammals and flightless birds have almost equal metabolic levels. The higher the metabolic rate in a group, the less it increases within increasing body size in this group.

Abstract

Analysis of metabolic scaling in currently living endothermic animal species allowed us to show how the relationship between body mass and the basal metabolic rate (BMR) has evolved in the history of endothermic vertebrates. We compared six taxonomic groups according to their energetic characteristics and the time of evolutionary divergence. We transformed the slope of the regression lines to the common value and analyzed three criteria for comparing BMR of different taxa regardless of body size. Correlation between average field metabolic rate (FMR) of the group and its average BMR was shown. We evaluated the efficiency of self-maintenance in ordinary life (defined BMR/FMR) in six main groups of endotherms. Our study has shown that metabolic scaling in the main groups of endothermic animals correlates with their evolutionary age: the younger the group, the higher the metabolic rate, but the rate increases more slowly with increasing body weight. We found negative linear relationship for scaling exponents and the allometric coefficient in five groups of endotherms: in units of mL O2/h per g, in relative units of allometric coefficients, and also in level or scaling elevation. Mammals that diverged from the main vertebrate stem earlier have a higher “b” exponent than later divergent birds. A new approach using three criteria for comparing BMR of different taxa regardless of body mass will be useful for many biological size-scaling relationships that follow the power function.

SUBMITTER: Gavrilov V

PROVIDER: S-EPMC9312277 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Basal metabolic rate (BMR) represents the minimum maintenance energy requirement of an endotherm and has far-reaching consequences for interactions between animals and their environments. Avian BMR exhibits considerable variation that is independent of body mass. Some long-distance migrants have been found to exhibit particularly high BMR, traditionally interpreted as being related to the energetic demands of long-distance migration. Here we use a global dataset to evaluate differences in BMR between migrants and non-migrants, and to examine the effects of environmental variables. The BMR of migrant species is significantly higher than that of non-migrants. Intriguingly, while the elevated BMR of migrants on their breeding grounds may reflect the metabolic machinery required for long-distance movements, an alternative (and statistically stronger) explanation is their occupation of predominantly cold high-latitude breeding areas. Among several environmental predictors, average annual temperature has the strongest effect on BMR, with a 50% reduction associated with a 20 degrees C gradient. The negative effects of temperature variables on BMR hold separately for migrants and non-migrants and are not due their different climatic associations. BMR in migrants shows a much lower degree of phylogenetic inertia. Our findings indicate that migratory tendency need not necessarily be invoked to explain the higher BMR of migrants. A weaker phylogenetic signal observed in migrants supports the notion of strong phenotypic flexibility in this group which facilitates migration-related BMR adjustments that occur above and beyond environmental conditions. In contrast to the findings of previous analyses of mammalian BMR, primary productivity, aridity or precipitation variability do not appear to be important environmental correlates of avian BMR. The strong effects of temperature-related variables and varying phylogenetic effects reiterate the importance of addressing both broad-scale and individual-scale variation for understanding the determinants of BMR.

Project description:BACKGROUND:Malagasy tenrecs belong to the Afrotherian clade of placental mammals and comprise three subfamilies divided in eight genera (Tenrecinae: Tenrec, Echinops, Setifer and Hemicentetes; Oryzorictinae: Oryzorictes, Limnogale and Microgale; Geogalinae:Geogale). The diversity of their morphology and incomplete taxon sampling made it difficult until now to resolve phylogenies based on either morphology or molecular data for this group. Therefore, in order to delineate the evolutionary history of this family, phylogenetic and dating analyses were performed on a four nuclear genes dataset (ADRA2B, AR, GHR and vWF) including all Malagasy tenrec genera. Moreover, the influence of both taxon sampling and data partitioning on the accuracy of the estimated ages were assessed. RESULTS:Within Afrotheria the vast majority of the nodes received a high support, including the grouping of hyrax with sea cow and the monophyly of both Afroinsectivora (Macroscelidea + Afrosoricida) and Afroinsectiphillia (Tubulidentata + Afroinsectivora). Strongly supported relationships were also recovered among all tenrec genera, allowing us to firmly establish the grouping of Geogale with Oryzorictinae, and to confirm the previously hypothesized nesting of Limnogale within the genus Microgale. The timeline of Malagasy tenrec diversification does not reflect a fast adaptive radiation after the arrival on Madagascar, indicating that morphological specializations have appeared over the whole evolutionary history of the family, and not just in a short period after colonization. In our analysis, age estimates at the root of a clade became older with increased taxon sampling of that clade. Moreover an augmentation of data partitions resulted in older age estimates as well, whereas standard deviations increased when more extreme partition schemes were used. CONCLUSION:Our results provide as yet the best resolved gene tree comprising all Malagasy tenrec genera, and may lead to a revision of tenrec taxonomy. A timeframe of tenrec evolution built on the basis of this solid phylogenetic framework showed that morphological specializations of the tenrecs may have been affected by environmental changes caused by climatic and/or subsequent colonization events. Analyses including various taxon sampling and data partitions allow us to point out some possible pitfalls that may lead to biased results in molecular dating; however, further analyses are needed to corroborate these observations.

Project description:1. The power-law dependence of metabolic rate on body mass has major implications at every level of ecological organization. However, the overwhelming majority of studies examining this relationship have used basal or resting metabolic rates, and/or have used data consisting of species-averaged masses and metabolic rates. Field metabolic rates are more ecologically relevant and are probably more directly subject to natural selection than basal rates. Individual rates might be more important than species-average rates in determining the outcome of ecological interactions, and hence selection. 2. We here provide the first comprehensive database of published field metabolic rates and body masses of individual birds and mammals, containing measurements of 1498 animals of 133 species in 28 orders. We used linear mixed-effects models to answer questions about the body mass scaling of metabolic rate and its taxonomic universality/heterogeneity that have become classic areas of controversy. Our statistical approach allows mean scaling exponents and taxonomic heterogeneity in scaling to be analysed in a unified way while simultaneously accounting for nonindependence in the data due to shared evolutionary history of related species. 3. The mean power-law scaling exponents of metabolic rate vs. body mass relationships were 0.71 [95% confidence intervals (CI) 0.625-0.795] for birds and 0.64 (95% CI 0.564-0.716) for mammals. However, these central tendencies obscured meaningful taxonomic heterogeneity in scaling exponents. The primary taxonomic level at which heterogeneity occurred was the order level. Substantial heterogeneity also occurred at the species level, a fact that cannot be revealed by species-averaged data sets used in prior work. Variability in scaling exponents at both order and species levels was comparable to or exceeded the differences 3/4-2/3 = 1/12 and 0.71-0.64. 4. Results are interpreted in the light of a variety of existing theories. In particular, results are consistent with the heat dissipation theory of Speakman & Król (2010) and provided some support for the metabolic levels boundary hypothesis of Glazier (2010). 5. Our analysis provides the first comprehensive empirical analysis of the scaling relationship between field metabolic rate and body mass in individual birds and mammals. Our data set is a valuable contribution to those interested in theories of the allometry of metabolic rates.

Dataset Information

Metabolic Scaling in Birds and Mammals: How Taxon Divergence Time, Phylogeny, and Metabolic Rate Affect the Relationship between Scaling Exponents and Intercepts

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