CoChat
Sign Up
Cited by 48Physiological and biochemical adaptationsEvolution and Paleontology StudiesChromosomal and Genetic Variations

The relationship between genome size and metabolic rate in extant vertebrates

Open access
Gardner, Jacob D., Laurin, Michel, Organ, Chris L.·2020·Philosophical Transactions of the Royal Society B: Biological Sciences
DOI 10.1098/rstb.2019.0146PMC PMC7017434

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Genome size has long been hypothesized to affect the metabolic rate in various groups of animals. The mechanism behind this proposed association is the nucleotypic effect, in which large nucleus and cell sizes influence cellular metabolism through surface area-to-volume ratios. Here, we provide a review of the recent literature on the relationship between genome size and metabolic rate. We also conduct an analysis using phylogenetic comparative methods and a large sample of extant vertebrates. We find no evidence that the effect of genome size improves upon models in explaining metabolic rate variation. Not surprisingly, our results show a strong positive relationship between metabolic rate and body mass, as well as a substantial difference in metabolic rate between endothermic and ectothermic vertebrates, controlling for body mass. The presence of endothermy can also explain elevated rate shifts in metabolic rate whereas genome size cannot. We further find no evidence for a punctuated model of evolution for metabolic rate. Our results do not rule out the possibility that genome size affects cellular physiology in some tissues, but they are consistent with previous research suggesting little support for a direct functional connection between genome size and basal metabolic rate in extant vertebrates. This article is part of the theme issue ‘Vertebrate palaeophysiology’.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1098/rstb.2019.0146

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Both loaches/Psilorhynchidae and progenetic miniatures inhabit physiologically demanding environments, which has been linked to selection for smaller genomes through the relationship between cell size, nuclear DNA content, and metabolic rate.

    “Both groups therefore inhabit physiologically demanding environments, which has been linked to selection for smaller genomes through the relationship between cell size, nuclear DNA content, and metabolic rate (e.g., refs. 45, 47, and 51–53).”

    From Convergent genome streamlining accompanies independent miniaturization in the world’s smallest fishes (2026) · cites this paper as [51]

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 33

  1. Hughes AL, Hughes MK. 1995 Small genomes for better flyers. Nature 377, 391. (doi:10.1038/377391a0) · DOI
  2. Gregory TR. 2005 Genome Size Evolution in Animals. In The Evolution of the Genome (ed TR Gregory), pp. 4-71. Boston: Elsevier Academic Press.
  3. Ji Y, DeWoody JA. 2017 Relationships Among Powered Flight, Metabolic Rate, Body Mass, Genome Size, and the Retrotransposon Complement of Volant Birds. Evol. Biol. 44, 261- 272. (doi:10.1007/s11692-016-9405-4) · DOI
  4. Uyeda JC, Pennell MW, Miller ET, Maia R, McClain CR. 2017 The Evolution of Energetic Scaling across the Vertebrate Tree of Life. Am. Nat. 190, 185-199. (doi:10.1086/692326) · DOI
  5. Smith JDL, Bickham JW, Gregory TR. 2013 Patterns of genome size diversity in bats (order Chiroptera). Genome 56, 457-472. (doi:10.1139/gen-2013-0046) · DOI
  6. Laurin M. 2010 The subjective nature of Linnaean categories and its impact in evolutionary biology and biodiversity studies. Contrib. Zool. 79, 131-146. (doi:10.1163/18759866- 07904001) · DOI
  7. Kozlowski J, Konarzewski M, Gawelczyk AT. 2003 Cell size as a link between noncoding DNA and metabolic rate scaling. Proc. Natl. Acad. Sci. U. S. A. 100, 14080-14085.
  8. Kapusta A, Suh A, Feschotte C. 2017 Dynamics of genome size evolution in birds and mammals. Proc. Natl. Acad. Sci. 114, E1460-E1469. (doi:10.1073/pnas.1616702114) · DOI · Paper page
  9. Hughes AL. 1999 Adaptive evolution of genes and genomes. Oxford: Oxford University Press.
  10. Zhang Q, Edwards SV. 2012 The Evolution of Intron Size in Amniotes: A Role for Powered Flight? Genome Biol. Evol. 4, 1033-1043. (doi:10.1093/gbe/evs070) · DOI
  11. Smith JDL, Gregory TR. 2009 The genome sizes of megabats (Chiroptera: Pteropodidae) are remarkably constrained. Biol. Lett. 5, 347-351. (doi:10.1098/rsbl.2009.0016) · DOI
  12. Organ CL, Brusatte SL, Stein K. 2009 Sauropod dinosaurs evolved moderately sized genomes unrelated to body size. Proc. R. Soc. Lond. B Biol. Sci. 276, 4303-4308. (doi:10.1098/rspb.2009.1343) · DOI
  13. Andrews CB, Mackenzie SA, Gregory TR. 2008 Genome size and wing parameters in passerine birds. Proc. R. Soc. B 276, 55-61.
  14. Wright Natalie A., Gregory T. Ryan, Witt Christopher C. 2014 Metabolic 'engines' of flight drive genome size reduction in birds. Proc. R. Soc. B Biol. Sci. 281, 20132780. (doi:10.1098/rspb.2013.2780) · DOI
  15. Gregory TR, Andrews CB, McGuire JA, Witt CC. 2009 The smallest avian genomes are found in hummingbirds. Proc. R. Soc. B Biol. Sci. 276, 3753-3757. (doi:10.1098/rspb.2009.1004) · DOI
  16. Organ CL, Shedlock AM, Meade A, Pagel M, Edwards SV. 2007 Origin of avian genome size and structure in non-avian dinosaurs. Nature 446, 180-184. (doi:10.1038/nature05621) · DOI
  17. Organ CL, Shedlock AM. 2009 Palaeogenomics of pterosaurs and the evolution of small genome size in flying vertebrates. Biol. Lett. 5, 47-50. (doi:10.1098/rsbl.2008.0491) · DOI
  18. Organ C, Struble M, Canoville A, de Buffrénil V, Laurin M. 2016 Macroevolution of genome size in sarcopterygians during the water-land transition. Comptes Rendus Palevol 15, 65- 73. (doi:10.1016/j.crpv.2015.09.003) · DOI
  19. Legendre LJ, Guénard G, Botha-Brink J, Cubo J. 2016 Palaeohistological Evidence for Ancestral High Metabolic Rate in Archosaurs. Syst. Biol. , syw033. (doi:10.1093/sysbio/syw033) · DOI
  20. Starostová Z, Kubicka L, Konarzewski M, Kozłowski J, Kratochvíl L. 2009 Cell size but not genome size affects scaling of metabolic rate in eyelid geckos. Am. Nat. 174, E100-105. (doi:10.1086/603610) · DOI
  21. Guénard G, Legendre P, Peres-Neto P. 2013 Phylogenetic eigenvector maps: a framework to model and predict species traits. Methods Ecol. Evol. 4, 1120-1131. (doi:10.1111/2041- 210X.12111) · DOI
  22. Grunmeier Orvil, D'Emic Michael D. 2019 Scaling of statically derived osteocyte lacunae in extant birds: implications for palaeophysiological reconstruction. Biol. Lett. 15, 20180837. (doi:10.1098/rsbl.2018.0837) · DOI
  23. D'Emic MD, Benson RBJ. 2013 Measurement, variation, and scaling of osteocyte lacunae: a case study in birds. Bone 57, 300-310. (doi:10.1016/j.bone.2013.08.010) · DOI
  24. Czarnoleski M, Labecka AM, Dragosz-Kluska D, Pis T, Pawlik K, Kapustka F, Kilarski WM, Kozłowski J. 2018 Concerted evolution of body mass and cell size: similar patterns among species of birds (Galliformes) and mammals (Rodentia). Biol. Open 7, bio029603. (doi:10.1242/bio.029603) · DOI
  25. Licht LE, Lowcock LA. 1991 Genome size and metabolic rate in salamanders. Comp. Biochem. Physiol. Part B Comp. Biochem. 100, 83-92. (doi:10.1016/0305-0491(91)90089-V) · DOI
  26. Gregory TR. 2003 Variation across amphibian species in the size of the nuclear genome supports a pluralistic, hierarchical approach to the C-value enigma. Biol. J. Linn. Soc. 79, 329-339. (doi:10.1046/j.1095-8312.2003.00191.x) · DOI
  27. Hermaniuk A, Rybacki M, Taylor JRE. 2017 Metabolic Rate of Diploid and Triploid Edible Frog Pelophylax esculentus Correlates Inversely with Cell Size in Tadpoles but Not in Frogs. Physiol. Biochem. Zool. PBZ 90, 230-239. (doi:10.1086/689408) · DOI
  28. Liedtke HC, Gower DJ, Wilkinson M, Gomez-Mestre I. 2018 Macroevolutionary shift in the size of amphibian genomes and the role of life history and climate. Nat. Ecol. Evol. 2, 1792- 1799. (doi:10.1038/s41559-018-0674-4) · DOI · Paper page
  29. Smith EM, Gregory TR. 2009 Patterns of genome size diversity in the ray-finned fishes. Hydrobiologia 625, 1-25. (doi:10.1007/s10750-009-9724-x) · DOI · Paper page
  30. Maciak S, Janko K, Kotusz J, Choleva L, Boroń A, Juchno D, Kujawa R, Kozłowski J, Konarzewski M. 2011 Standard Metabolic Rate (SMR) is inversely related to erythrocyte and genome size in allopolyploid fish of the Cobitis taenia hybrid complex. Funct. Ecol. 25, 1072-1078. (doi:10.1111/j.1365-2435.2011.01870.x) · DOI
  31. Baker J, Meade A, Pagel M, Venditti C. 2016 Positive phenotypic selection inferred from phylogenies. Biol. J. Linn. Soc. 118, 95-115. (doi:10.1111/bij.12649) · DOI
  32. Baker J, Venditti C. 2019 Rapid Change in Mammalian Eye Shape Is Explained by Activity Pattern. Curr. Biol. 29, 1082-1088.e3. (doi:10.1016/j.cub.2019.02.017) · DOI
  33. Atkinson QD, Meade A, Venditti C, Greenhill SJ, Pagel M. 2008 Languages Evolve in Punctuational Bursts. Science 319, 588-588. (doi:10.1126/science.1149683) · DOI

Cited by

Sorted by citations

Authors
Gardner, J. D., Laurin, M., & Organ, C. L.
Affiliations
  • Montana State University (US)
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
  • Gardner, Jacob D.
  • Laurin, Michel
  • Organ, Chris L.
ORCID
Venue
Philosophical Transactions of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2020-01-13
Volume
375
Issue
1793
Pages
20190146
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
DOI
10.1098/rstb.2019.0146
PMC
PMC7017434
OpenAlex
W2999855442
Cited by
48
References
2
Citations by year
2026: 4 · 2025: 9 · 2024: 6 · 2023: 5 · 2022: 11 · 2021: 8 · 2020: 5
FWCI
3.78
Type
journal article
Language
en
Open access
Licence
Locations
  • Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Montana State University ScholarWorks (Montana State University) (submittedVersion, cc-by)
  • HAL (submittedVersion, other-oa)
Topics
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords
genome size, basal metabolic rate, surface-to-volume ratio, endothermy, ectothermy, body mass, phylogenetic comparative analysis, punctuated evolution, cellular metabolism
MeSH terms
Animals, Basal Metabolism, Body Temperature Regulation, Biological Evolution, Phylogeny, Vertebrates, Genome Size

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review