Skip to main content
Genetics logoLink to Genetics
. 2001 Sep;159(1):267–277. doi: 10.1093/genetics/159.1.267

The quantitative genetics of maximal and basal rates of oxygen consumption in mice.

M R Dohm 1, J P Hayes 1, T Garland Jr 1
PMCID: PMC1461780  PMID: 11560903

Abstract

A positive genetic correlation between basal metabolic rate (BMR) and maximal (VO(2)max) rate of oxygen consumption is a key assumption of the aerobic capacity model for the evolution of endothermy. We estimated the genetic (V(A), additive, and V(D), dominance), prenatal (V(N)), and postnatal common environmental (V(C)) contributions to individual differences in metabolic rates and body mass for a genetically heterogeneous laboratory strain of house mice (Mus domesticus). Our breeding design did not allow the simultaneous estimation of V(D) and V(N). Regardless of whether V(D) or V(N) was assumed, estimates of V(A) were negative under the full models. Hence, we fitted reduced models (e.g., V(A) + V(N) + V(E) or V(A) + V(E)) and obtained new variance estimates. For reduced models, narrow-sense heritability (h(2)(N)) for BMR was <0.1, but estimates of h(2)(N) for VO(2)max were higher. When estimated with the V(A) + V(E) model, the additive genetic covariance between VO(2)max and BMR was positive and statistically different from zero. This result offers tentative support for the aerobic capacity model for the evolution of vertebrate energetics. However, constraints imposed on the genetic model may cause our estimates of additive variance and covariance to be biased, so our results should be interpreted with caution and tested via selection experiments.

Full Text

The Full Text of this article is available as a PDF (129.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bagatto B., Crossley D. A., 2nd, Burggren W. W. Physiological variability in neonatal armadillo quadruplets: within- and between-litter differences. J Exp Biol. 2000 Jun;203(Pt 11):1733–1740. doi: 10.1242/jeb.203.11.1733. [DOI] [PubMed] [Google Scholar]
  2. Bennett A. F., Ruben J. A. Endothermy and activity in vertebrates. Science. 1979 Nov 9;206(4419):649–654. doi: 10.1126/science.493968. [DOI] [PubMed] [Google Scholar]
  3. Bennett A. F. The evolution of activity capacity. J Exp Biol. 1991 Oct;160:1–23. doi: 10.1242/jeb.160.1.1. [DOI] [PubMed] [Google Scholar]
  4. Bogardus C., Lillioja S., Ravussin E., Abbott W., Zawadzki J. K., Young A., Knowler W. C., Jacobowitz R., Moll P. P. Familial dependence of the resting metabolic rate. N Engl J Med. 1986 Jul 10;315(2):96–100. doi: 10.1056/NEJM198607103150205. [DOI] [PubMed] [Google Scholar]
  5. Bouchard C., An P., Rice T., Skinner J. S., Wilmore J. H., Gagnon J., Pérusse L., Leon A. S., Rao D. C. Familial aggregation of VO(2max) response to exercise training: results from the HERITAGE Family Study. J Appl Physiol (1985) 1999 Sep;87(3):1003–1008. doi: 10.1152/jappl.1999.87.3.1003. [DOI] [PubMed] [Google Scholar]
  6. Carter P. A., Garland T., Jr, Dohm M. R., Hayes J. P. Genetic variation and correlations between genotype and locomotor physiology in outbred laboratory house mice (Mus domesticus). Comp Biochem Physiol A Mol Integr Physiol. 1999 Jun;123(2):155–162. doi: 10.1016/s1095-6433(99)00044-6. [DOI] [PubMed] [Google Scholar]
  7. Chappell M. A., Snyder L. R. Biochemical and physiological correlates of deer mouse alpha-chain hemoglobin polymorphisms. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5484–5488. doi: 10.1073/pnas.81.17.5484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Damme K., Pirchner F., Willeke H., Eichinger H. Fasting metabolic rate in hens. 2. Strain differences and heritability estimates. Poult Sci. 1986 Apr;65(4):616–620. doi: 10.3382/ps.0650616. [DOI] [PubMed] [Google Scholar]
  9. Dohm M. R., Richardson C. S., Garland T., Jr Exercise physiology of wild and random-bred laboratory house mice and their reciprocal hybrids. Am J Physiol. 1994 Oct;267(4 Pt 2):R1098–R1108. doi: 10.1152/ajpregu.1994.267.4.R1098. [DOI] [PubMed] [Google Scholar]
  10. Friedman W. A., Garland T., Jr, Dohm M. R. Individual variation in locomotor behavior and maximal oxygen consumption in mice. Physiol Behav. 1992 Jul;52(1):97–104. doi: 10.1016/0031-9384(92)90438-8. [DOI] [PubMed] [Google Scholar]
  11. Garland T., Jr, Bennett A. F. Quantitative genetics of maximal oxygen consumption in a garter snake. Am J Physiol. 1990 Nov;259(5 Pt 2):R986–R992. doi: 10.1152/ajpregu.1990.259.5.R986. [DOI] [PubMed] [Google Scholar]
  12. Garland T., Jr, Carter P. A. Evolutionary physiology. Annu Rev Physiol. 1994;56:579–621. doi: 10.1146/annurev.ph.56.030194.003051. [DOI] [PubMed] [Google Scholar]
  13. Garland T., Jr, Gleeson T. T., Aronovitz B. A., Richardson C. S., Dohm M. R. Maximal sprint speeds and muscle fiber composition of wild and laboratory house mice. Physiol Behav. 1995 Nov;58(5):869–876. doi: 10.1016/0031-9384(95)00148-c. [DOI] [PubMed] [Google Scholar]
  14. Hill R. W. Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J Appl Physiol. 1972 Aug;33(2):261–263. doi: 10.1152/jappl.1972.33.2.261. [DOI] [PubMed] [Google Scholar]
  15. Hinds D. S., Baudinette R. V., MacMillen R. E., Halpern E. A. Maximum metabolism and the aerobic factorial scope of endotherms. J Exp Biol. 1993 Sep;182:41–56. doi: 10.1242/jeb.182.1.41. [DOI] [PubMed] [Google Scholar]
  16. Lacy R. C., Lynch C. B. Quantitative Genetic Analysis of Temperature Regulation in MUS MUSCULUS. I. Partitioning of Variance. Genetics. 1979 Apr;91(4):743–753. doi: 10.1093/genetics/91.4.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lesage R., Simoneau J. A., Jobin J., Leblanc J., Bouchard C. Familial resemblance in maximal heart rate, blood lactate and aerobic power. Hum Hered. 1985;35(3):182–189. doi: 10.1159/000153540. [DOI] [PubMed] [Google Scholar]
  18. Moody D. E., Pomp D., Nielsen M. K., Van Vleck L. D. Identification of quantitative trait loci influencing traits related to energy balance in selection and inbred lines of mice. Genetics. 1999 Jun;152(2):699–711. doi: 10.1093/genetics/152.2.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Moody D. E., Pomp D., Nielsen M. K. Variability in metabolic rate, feed intake and fatness among selection and inbred lines of mice. Genet Res. 1997 Dec;70(3):225–235. doi: 10.1017/s0016672397003017. [DOI] [PubMed] [Google Scholar]
  20. Rhees B. K., Ernst C. A., Miao C. H., Atchley W. R. Uterine and postnatal maternal effects in mice selected for differential rate of early development. Genetics. 1999 Oct;153(2):905–917. doi: 10.1093/genetics/153.2.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rice M. C., O'Brien S. J. Genetic variance of laboratory outbred Swiss mice. Nature. 1980 Jan 10;283(5743):157–161. doi: 10.1038/283157a0. [DOI] [PubMed] [Google Scholar]
  22. Rice T., Tremblay A., Dériaz O., Pérusse L., Rao D. C., Bouchard C. Genetic pleiotropy for resting metabolic rate with fat-free mass and fat mass: the Québec Family Study. Obes Res. 1996 Mar;4(2):125–131. doi: 10.1002/j.1550-8528.1996.tb00524.x. [DOI] [PubMed] [Google Scholar]
  23. Riska B., Atchley W. R., Rutledge J. J. A genetic analysis of targeted growth in mice. Genetics. 1984 May;107(1):79–101. doi: 10.1093/genetics/107.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ruben J. The evolution of endothermy in mammals and birds: from physiology to fossils. Annu Rev Physiol. 1995;57:69–95. doi: 10.1146/annurev.ph.57.030195.000441. [DOI] [PubMed] [Google Scholar]
  25. SCHLESINGER K., MORDKOFF A. M. LOCOMOTOR ACTIVITY AND OXYGEN CONSUMPTION. VARIABILITY IN TWO INBRED STRAINS OF MICE AND THEIR F HYBRIDS. J Hered. 1963 Jul-Aug;54:177–182. doi: 10.1093/jhered/54.4.177. [DOI] [PubMed] [Google Scholar]
  26. Sacher G. A., Duffy P. H. Genetic relation of life span to metabolic rate for inbred mouse strains and their hybrids. Fed Proc. 1979 Feb;38(2):184–188. [PubMed] [Google Scholar]
  27. Swallow J. G., Carter P. A., Garland T., Jr Artificial selection for increased wheel-running behavior in house mice. Behav Genet. 1998 May;28(3):227–237. doi: 10.1023/a:1021479331779. [DOI] [PubMed] [Google Scholar]
  28. Swallow J. G., Garland T., Jr, Carter P. A., Zhan W. Z., Sieck G. C. Effects of voluntary activity and genetic selection on aerobic capacity in house mice (Mus domesticus). J Appl Physiol (1985) 1998 Jan;84(1):69–76. doi: 10.1152/jappl.1998.84.1.69. [DOI] [PubMed] [Google Scholar]
  29. Wagner P. D. Determinants of maximal oxygen transport and utilization. Annu Rev Physiol. 1996;58:21–50. doi: 10.1146/annurev.ph.58.030196.000321. [DOI] [PubMed] [Google Scholar]
  30. Wei M., van der Werf J. H. Animal model estimation of additive and dominance variances in egg production traits of poultry. J Anim Sci. 1993 Jan;71(1):57–65. doi: 10.2527/1993.71157x. [DOI] [PubMed] [Google Scholar]
  31. Weibel E. R., Taylor C. R., Weber J. M., Vock R., Roberts T. J., Hoppeler H. Design of the oxygen and substrate pathways. VII. Different structural limits for oxygen and substrate supply to muscle mitochondria. J Exp Biol. 1996 Aug;199(Pt 8):1699–1709. doi: 10.1242/jeb.199.8.1699. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES