Peto's paradox and the promise of comparative oncology

doi:10.1098/rstb.2014.0177

. 2015 Jul 19;370(1673):20140177.

doi: 10.1098/rstb.2014.0177.

Peto's paradox and the promise of comparative oncology

Leonard Nunney¹, Carlo C Maley², Matthew Breen³, Michael E Hochberg⁴, Joshua D Schiffman⁵

Affiliations

¹ Department of Biology, University of California Riverside, CA 92521, USA.
² Biodesign Institute, Arizona State University, Tempe, AZ 85287, USA Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA 94143, USA Centre for Evolution and Cancer, Institute for Cancer Research, London, UK.
³ Department of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27695, USA Center for Comparative Medicine and Translational Research, North Carolina State University, Raleigh, NC 27695, USA Center for Human Health and the Environment, North Carolina State University, Raleigh, NC 27695, USA Genetics Program, Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27514, USA.
⁴ Institut des Sciences de l'Evolution, Université Montpellier, UMR5554 du CNRS, Montpellier 34095, France Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA.
⁵ Primary Children's Hospital (Intermountain Healthcare) and Huntsman Cancer Institute, Departments of Pediatrics and Oncological Sciences, University of Utah, Salt Lake City, UT 84112, USA [email protected].

PMID: 26056361
PMCID: PMC4581022
DOI: 10.1098/rstb.2014.0177

Peto's paradox and the promise of comparative oncology

Leonard Nunney et al. Philos Trans R Soc Lond B Biol Sci. 2015.

. 2015 Jul 19;370(1673):20140177.

doi: 10.1098/rstb.2014.0177.

Authors

Leonard Nunney¹, Carlo C Maley², Matthew Breen³, Michael E Hochberg⁴, Joshua D Schiffman⁵

Affiliations

¹ Department of Biology, University of California Riverside, CA 92521, USA.
² Biodesign Institute, Arizona State University, Tempe, AZ 85287, USA Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA 94143, USA Centre for Evolution and Cancer, Institute for Cancer Research, London, UK.
³ Department of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27695, USA Center for Comparative Medicine and Translational Research, North Carolina State University, Raleigh, NC 27695, USA Center for Human Health and the Environment, North Carolina State University, Raleigh, NC 27695, USA Genetics Program, Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27514, USA.
⁴ Institut des Sciences de l'Evolution, Université Montpellier, UMR5554 du CNRS, Montpellier 34095, France Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA.
⁵ Primary Children's Hospital (Intermountain Healthcare) and Huntsman Cancer Institute, Departments of Pediatrics and Oncological Sciences, University of Utah, Salt Lake City, UT 84112, USA [email protected].

PMID: 26056361
PMCID: PMC4581022
DOI: 10.1098/rstb.2014.0177

Abstract

The past several decades have seen a paradigm shift with the integration of evolutionary thinking into studying cancer. The evolutionary lens is most commonly employed in understanding cancer emergence, tumour growth and metastasis, but there is an increasing realization that cancer defences both between tissues within the individual and between species have been influenced by natural selection. This special issue focuses on discoveries of these deeper evolutionary phenomena in the emerging area of 'comparative oncology'. Comparing cancer dynamics in different tissues or species can lead to insights into how biology and ecology have led to differences in carcinogenesis, and the diversity, incidence and lethality of cancers. In this introduction to the special issue, we review the history of the field and outline how the contributions use empirical, comparative and theoretical approaches to address the processes and patterns associated with 'Peto's paradox', the lack of a statistical relationship of cancer incidence with body size and longevity. This burgeoning area of research can help us understand that cancer is not only a disease but is also a driving force in biological systems and species life histories. Comparative oncology will be key to understanding globally important health issues, including cancer epidemiology, prevention and improved therapies.

Keywords: Peto's paradox; cancer; comparative oncology; evolution; life-history theory; modelling.

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Figures

**Figure 1.**
The increasing number of citations to articles with ‘cancer’ and ‘evolution’ (or ‘evolutionary’) in the title from 1970 to 2014. Data from Web of Science (webofknowledge.com). (Online version in colour.)

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References

1. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144, 646–674. (10.1016/j.cell.2011.02.013) - DOI - PubMed
1. Aktipis CA, Boddy AM, Jansen G, Hibner U, Hochberg ME, Maley CC, Wilkinson GS. 2015. Cancer across the tree of life: cooperation and cheating in multicellularity. Phil. Trans. R. Soc. B 370, 20140219 (10.1098/rstb.2014.0219) - DOI - PMC - PubMed
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1. Nunney L. 1999. Lineage selection: natural selection for long-term benefit. In. Levels of selection in evolution (ed. L Keller), pp. 238–258.

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[1] Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144, 646–674. (10.1016/j.cell.2011.02.013) - DOI - PubMed

[2] Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144, 646–674. (10.1016/j.cell.2011.02.013) - DOI - PubMed

[3] Aktipis CA, Boddy AM, Jansen G, Hibner U, Hochberg ME, Maley CC, Wilkinson GS. 2015. Cancer across the tree of life: cooperation and cheating in multicellularity. Phil. Trans. R. Soc. B 370, 20140219 (10.1098/rstb.2014.0219) - DOI - PMC - PubMed

[4] Aktipis CA, Boddy AM, Jansen G, Hibner U, Hochberg ME, Maley CC, Wilkinson GS. 2015. Cancer across the tree of life: cooperation and cheating in multicellularity. Phil. Trans. R. Soc. B 370, 20140219 (10.1098/rstb.2014.0219) - DOI - PMC - PubMed

[5] Nunney L, Muir B. 2015. Peto's paradox and the hallmarks of cancer: constructing an evolutionary framework for understanding the incidence of cancer. Phil. Trans. R. Soc. B 370, 20150161 (10.1098/rstb.2015.0161) - DOI - PMC - PubMed

[6] Nunney L, Muir B. 2015. Peto's paradox and the hallmarks of cancer: constructing an evolutionary framework for understanding the incidence of cancer. Phil. Trans. R. Soc. B 370, 20150161 (10.1098/rstb.2015.0161) - DOI - PMC - PubMed

[7] Nunney L. 1999. Lineage selection and the evolution of multistage carcinogenesis. Proc. R. Soc. Lond. B 266, 493–498. (10.1098/rspb.1999.0664) - DOI - PMC - PubMed

[8] Nunney L. 1999. Lineage selection and the evolution of multistage carcinogenesis. Proc. R. Soc. Lond. B 266, 493–498. (10.1098/rspb.1999.0664) - DOI - PMC - PubMed

[9] Nunney L. 1999. Lineage selection: natural selection for long-term benefit. In. Levels of selection in evolution (ed. L Keller), pp. 238–258.

[10] Nunney L. 1999. Lineage selection: natural selection for long-term benefit. In. Levels of selection in evolution (ed. L Keller), pp. 238–258.

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Peto's paradox and the promise of comparative oncology

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Peto's paradox and the promise of comparative oncology

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