skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Solutions to Peto's paradox revealed by mathematical modelling and cross-species cancer gene analysis

Abstract

Whales have 1000-fold more cells than humans and mice have 1000-fold fewer; however, cancer risk across species does not increase with the number of somatic cells and the lifespan of the organism. This observation is known as Peto's paradox. How much would evolution have to change the parameters of somatic evolution in order to equalize the cancer risk between species that differ by orders of magnitude in size? Analysis of previously published models of colorectal cancer suggests that a two- to three-fold decrease in the mutation rate or stem cell division rate is enough to reduce a whale's cancer risk to that of a human. Similarly, the addition of one to two required tumour-suppressor gene mutations would also be sufficient. Also, we surveyed mammalian genomes and did not find a positive correlation of tumour-suppressor genes with increasing body mass and longevity. However, we found evidence of the amplification of TP53 in elephants, MAL in horses and FBXO31 in microbats, which might explain Peto's paradox in those species. Lastly, exploring parameters that evolution may have fine-tuned in large, long-lived organisms will help guide future experiments to reveal the underlying biology responsible for Peto's paradox and guide cancer prevention in humans.

Authors:
 [1];  [2];  [3];  [4]
  1. Univ. of Pennsylvania, Philadelphia, PA (United States). Genomics and Computational Biology Graduate Program
  2. Queen Mary University of London, London (United Kingdom). Evolution and Cancer Laboratory, Barts Cancer Institute, Barts and the London School of Medicine and Dentistry
  3. Univ. of Pennsylvania, Philadelphia, PA (United States). Department of Pathology and Laboratory Medicine
  4. Arizona State Univ., Tempe, AZ (United States). Biodesign Institute, School of Life Sciences; Univ. of California, San Francisco, CA (United States). Center for Evolution and Cancer
Publication Date:
Research Org.:
Univ. of Pennsylvania, Philadelphia, PA (United States)
Sponsoring Org.:
USDOE; National Institutes of Health (NIH)
OSTI Identifier:
1343568
Grant/Contract Number:  
FG02-97ER25308
Resource Type:
Accepted Manuscript
Journal Name:
Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences
Additional Journal Information:
Journal Volume: 370; Journal Issue: 1673; Journal ID: ISSN 0962-8436
Publisher:
The Royal Society Publishing
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Peto’s paradox; evolution; cancer; tumour suppression; algebraic model; Wright–Fisher model

Citation Formats

Caulin, Aleah F., Graham, Trevor A., Wang, Li-San, and Maley, Carlo C. Solutions to Peto's paradox revealed by mathematical modelling and cross-species cancer gene analysis. United States: N. p., 2015. Web. doi:10.1098/rstb.2014.0222.
Caulin, Aleah F., Graham, Trevor A., Wang, Li-San, & Maley, Carlo C. Solutions to Peto's paradox revealed by mathematical modelling and cross-species cancer gene analysis. United States. doi:https://doi.org/10.1098/rstb.2014.0222
Caulin, Aleah F., Graham, Trevor A., Wang, Li-San, and Maley, Carlo C. Mon . "Solutions to Peto's paradox revealed by mathematical modelling and cross-species cancer gene analysis". United States. doi:https://doi.org/10.1098/rstb.2014.0222. https://www.osti.gov/servlets/purl/1343568.
@article{osti_1343568,
title = {Solutions to Peto's paradox revealed by mathematical modelling and cross-species cancer gene analysis},
author = {Caulin, Aleah F. and Graham, Trevor A. and Wang, Li-San and Maley, Carlo C.},
abstractNote = {Whales have 1000-fold more cells than humans and mice have 1000-fold fewer; however, cancer risk across species does not increase with the number of somatic cells and the lifespan of the organism. This observation is known as Peto's paradox. How much would evolution have to change the parameters of somatic evolution in order to equalize the cancer risk between species that differ by orders of magnitude in size? Analysis of previously published models of colorectal cancer suggests that a two- to three-fold decrease in the mutation rate or stem cell division rate is enough to reduce a whale's cancer risk to that of a human. Similarly, the addition of one to two required tumour-suppressor gene mutations would also be sufficient. Also, we surveyed mammalian genomes and did not find a positive correlation of tumour-suppressor genes with increasing body mass and longevity. However, we found evidence of the amplification of TP53 in elephants, MAL in horses and FBXO31 in microbats, which might explain Peto's paradox in those species. Lastly, exploring parameters that evolution may have fine-tuned in large, long-lived organisms will help guide future experiments to reveal the underlying biology responsible for Peto's paradox and guide cancer prevention in humans.},
doi = {10.1098/rstb.2014.0222},
journal = {Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences},
number = 1673,
volume = 370,
place = {United States},
year = {2015},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 9 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Peto's Paradox: evolution's prescription for cancer prevention
journal, April 2011


The real war on cancer: the evolutionary dynamics of cancer suppression
journal, October 2012


Natural resistance to cancers: a Darwinian hypothesis to explain Peto’s paradox
journal, September 2012


Genetic Progression and the Waiting Time to Cancer
journal, January 2007


A simple algebraic cancer equation: calculating how cancers may arise with normal mutation rates
journal, January 2010


Automatic Retrieval of Bone Fracture Knowledge Using Natural Language Processing
journal, October 2012


Spatial structure increases the waiting time for cancer
journal, November 2011


Lineage selection and the evolution of multistage carcinogenesis
journal, March 1999

  • Nunney, Leonard
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 266, Issue 1418
  • DOI: 10.1098/rspb.1999.0664

Pretumor Progression
journal, April 2004


A database of vertebrate longevity records and their relation to other life‐history traits
journal, July 2009


Cancer in wildlife, a case study: beluga from the St. Lawrence estuary, Québec, Canada.
journal, March 2002

  • Martineau, Daniel; Lemberger, Karin; Dallaire, André
  • Environmental Health Perspectives, Vol. 110, Issue 3
  • DOI: 10.1289/ehp.02110285

Marine Mammal Neoplasia: A Review
journal, November 2006


The null oncogene hypothesis and protection from cancer
journal, January 2002


Gatekeepers and caretakers
journal, April 1997

  • Kinzler, Kenneth W.; Vogelstein, Bert
  • Nature, Vol. 386, Issue 6627
  • DOI: 10.1038/386761a0

Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa
journal, May 2010


CancerGenes: a gene selection resource for cancer genome projects
journal, January 2007

  • Higgins, M. E.; Claremont, M.; Major, J. E.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl811

Genome analysis reveals insights into physiology and longevity of the Brandt’s bat Myotis brandtii
journal, August 2013

  • Seim, Inge; Fang, Xiaodong; Xiong, Zhiqiang
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3212

F-box protein FBXO31 mediates cyclin D1 degradation to induce G1 arrest after DNA damage
journal, May 2009

  • Santra, Manas K.; Wajapeyee, Narendra; Green, Michael R.
  • Nature, Vol. 459, Issue 7247
  • DOI: 10.1038/nature08011

p53 mutations in human cancers
journal, July 1991


'Super p53' mice exhibit enhanced DNA damage response, are tumor resistant and age normally
journal, November 2002

  • García-Cao, Isabel; García-Cao, Marta; Martín-Caballero, Juan
  • The EMBO Journal, Vol. 21, Issue 22
  • DOI: 10.1093/emboj/cdf595

Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF).
journal, December 1987


cDNA cloning and sequence of MAL, a hydrophobic protein associated with human T-cell differentiation.
journal, April 1987

  • Alonso, M. A.; Weissman, S. M.
  • Proceedings of the National Academy of Sciences, Vol. 84, Issue 7
  • DOI: 10.1073/pnas.84.7.1997

VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells
journal, May 1999

  • Cheong, K. H.; Zacchetti, D.; Schneeberger, E. E.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 11
  • DOI: 10.1073/pnas.96.11.6241

Substitution of the Two Carboxyl-terminal Serines by Alanine Causes Retention of MAL, a Component of the Apical Sorting Machinery, in the Endoplasmic Reticulum
journal, June 1999

  • Puertollano, Rosa; Alonso, Miguel A.
  • Biochemical and Biophysical Research Communications, Vol. 260, Issue 1
  • DOI: 10.1006/bbrc.1999.0876

Targeting of MAL, a Putative Element of the Apical Sorting Machinery, to Glycolipid-Enriched Membranes Requires a Pre-Golgi Sorting Event
journal, January 1999

  • Puertollano, Rosa; Alonso, Miguel A.
  • Biochemical and Biophysical Research Communications, Vol. 254, Issue 3
  • DOI: 10.1006/bbrc.1998.0122

Inactivation of the MAL Gene in Breast Cancer Is a Common Event That Predicts Benefit from Adjuvant Chemotherapy
journal, February 2009


Hypermethylated MAL gene – a silent marker of early colon tumorigenesis
journal, January 2008

  • Lind, Guro E.; Ahlquist, Terje; Kolberg, Matthias
  • Journal of Translational Medicine, Vol. 6, Issue 1
  • DOI: 10.1186/1479-5876-6-13

MAL gene expression in esophageal cancer suppresses motility, invasion and tumorigenicity and enhances apoptosis through the Fas pathway
journal, May 2003


Epigenetic silencing of MAL, a putative tumor suppressor gene, can contribute to human epithelium cell carcinoma
journal, January 2010


The Nature of the Principal Type 1 Interferon-Producing Cells in Human Blood
journal, June 1999


Integration of interferon-α/β signalling to p53 responses in tumour suppression and antiviral defence
journal, July 2003

  • Takaoka, Akinori; Hayakawa, Sumio; Yanai, Hideyuki
  • Nature, Vol. 424, Issue 6948
  • DOI: 10.1038/nature01850

Comparative lesion sequencing provides insights into tumor evolution
journal, March 2008

  • Jones, S.; Chen, W. -d.; Parmigiani, G.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 11
  • DOI: 10.1073/pnas.0712345105

Intestinal Crypt Homeostasis Results from Neutral Competition between Symmetrically Dividing Lgr5 Stem Cells
journal, October 2010


Cancer selection
journal, March 2003

  • Leroi, Armand M.; Koufopanou, Vassiliki; Burt, Austin
  • Nature Reviews Cancer, Vol. 3, Issue 3
  • DOI: 10.1038/nrc1016

Evolution of cooperation among tumor cells
journal, August 2006

  • Axelrod, R.; Axelrod, D. E.; Pienta, K. J.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 36
  • DOI: 10.1073/pnas.0606053103

The clonal evolution of tumor cell populations
journal, October 1976


Telomerase activity coevolves with body mass not lifespan
journal, February 2007


Coevolution of telomerase activity and body mass in mammals: From mice to beavers
journal, January 2009


Comparative genetics of longevity and cancer: insights from long-lived rodents
journal, July 2014

  • Gorbunova, Vera; Seluanov, Andrei; Zhang, Zhengdong
  • Nature Reviews Genetics, Vol. 15, Issue 8
  • DOI: 10.1038/nrg3728

Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat
journal, October 2009

  • Seluanov, A.; Hine, C.; Azpurua, J.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 46
  • DOI: 10.1073/pnas.0905252106

Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan
journal, December 2008


High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat
journal, June 2013

  • Tian, Xiao; Azpurua, Jorge; Hine, Christopher
  • Nature, Vol. 499, Issue 7458
  • DOI: 10.1038/nature12234

Mutation selection and the natural history of cancer
journal, May 1975


The evolutionary dynamics of cancer prevention
journal, August 2010

  • Gatenby, Robert A.; Gillies, Robert J.; Brown, Joel S.
  • Nature Reviews Cancer, Vol. 10, Issue 8
  • DOI: 10.1038/nrc2892

CT Evaluation of the Colon: Inflammatory Disease
journal, March 2000


Investigating stem cells in human colon by using methylation patterns
journal, August 2001

  • Yatabe, Y.; Tavare, S.; Shibata, D.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 19
  • DOI: 10.1073/pnas.191225998

Microcomputed tomography colonography for polyp detection in an in vivo mouse tumor model
journal, February 2005

  • Pickhardt, P. J.; Halberg, R. B.; Taylor, A. J.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 9
  • DOI: 10.1073/pnas.0409915102

Genome and genetic resources from the Cancer Genome Anatomy Project
journal, April 2001


The delayed rise of present-day mammals
journal, March 2007

  • Bininda-Emonds, Olaf R. P.; Cardillo, Marcel; Jones, Kate E.
  • Nature, Vol. 446, Issue 7135
  • DOI: 10.1038/nature05634

Genomic Divergences between Humans and Other Hominoids and the Effective Population Size of the Common Ancestor of Humans and Chimpanzees
journal, February 2001

  • Chen, Feng-Chi; Li, Wen-Hsiung
  • The American Journal of Human Genetics, Vol. 68, Issue 2
  • DOI: 10.1086/318206

Evolutionary and Biomedical Insights from the Rhesus Macaque Genome
journal, April 2007


Using genomic data to unravel the root of the placental mammal phylogeny
journal, March 2007

  • Murphy, W. J.; Pringle, T. H.; Crider, T. A.
  • Genome Research, Vol. 17, Issue 4
  • DOI: 10.1101/gr.5918807

Genetic evidence for complex speciation of humans and chimpanzees
journal, May 2006

  • Patterson, Nick; Richter, Daniel J.; Gnerre, Sante
  • Nature, Vol. 441, Issue 7097
  • DOI: 10.1038/nature04789

Body Mass of Late Quaternary Mammals
dataset, January 2004

  • Scales, NCEAS 2182: Smith: Body Size In Ecology And Paleoecology: Linking Pattern And Process Across Spatial, Temporal And Taxonomic; Smith, Felisa; Synthesis, National Center For Ecological Analysis And
  • KNB Data Repository
  • DOI: 10.5063/aa/nceas.177.3

The nature of the principal type 1 interferon-producing cells in human blood
journal, January 2000


    Works referencing / citing this record:

    All's well that ends well: why large species have short telomeres
    journal, January 2018

    • Risques, Rosa Ana; Promislow, Daniel E. L.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 373, Issue 1741
    • DOI: 10.1098/rstb.2016.0448

    Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF).
    journal, December 1987


    Targeting of MAL, a Putative Element of the Apical Sorting Machinery, to Glycolipid-Enriched Membranes Requires a Pre-Golgi Sorting Event
    journal, January 1999

    • Puertollano, Rosa; Alonso, Miguel A.
    • Biochemical and Biophysical Research Communications, Vol. 254, Issue 3
    • DOI: 10.1006/bbrc.1998.0122

    Substitution of the Two Carboxyl-terminal Serines by Alanine Causes Retention of MAL, a Component of the Apical Sorting Machinery, in the Endoplasmic Reticulum
    journal, June 1999

    • Puertollano, Rosa; Alonso, Miguel A.
    • Biochemical and Biophysical Research Communications, Vol. 260, Issue 1
    • DOI: 10.1006/bbrc.1999.0876

    Automatic Retrieval of Bone Fracture Knowledge Using Natural Language Processing
    journal, October 2012


    Intestinal Crypt Homeostasis Results from Neutral Competition between Symmetrically Dividing Lgr5 Stem Cells
    journal, October 2010


    Coevolution of telomerase activity and body mass in mammals: From mice to beavers
    journal, January 2009


    Peto's Paradox: evolution's prescription for cancer prevention
    journal, April 2011


    Pretumor Progression
    journal, April 2004


    Mutation selection and the natural history of cancer
    journal, May 1975


    Gatekeepers and caretakers
    journal, April 1997

    • Kinzler, Kenneth W.; Vogelstein, Bert
    • Nature, Vol. 386, Issue 6627
    • DOI: 10.1038/386761a0

    Integration of interferon-α/β signalling to p53 responses in tumour suppression and antiviral defence
    journal, July 2003

    • Takaoka, Akinori; Hayakawa, Sumio; Yanai, Hideyuki
    • Nature, Vol. 424, Issue 6948
    • DOI: 10.1038/nature01850

    Genetic evidence for complex speciation of humans and chimpanzees
    journal, May 2006

    • Patterson, Nick; Richter, Daniel J.; Gnerre, Sante
    • Nature, Vol. 441, Issue 7097
    • DOI: 10.1038/nature04789

    The delayed rise of present-day mammals
    journal, March 2007

    • Bininda-Emonds, Olaf R. P.; Cardillo, Marcel; Jones, Kate E.
    • Nature, Vol. 446, Issue 7135
    • DOI: 10.1038/nature05634

    F-box protein FBXO31 mediates cyclin D1 degradation to induce G1 arrest after DNA damage
    journal, May 2009

    • Santra, Manas K.; Wajapeyee, Narendra; Green, Michael R.
    • Nature, Vol. 459, Issue 7247
    • DOI: 10.1038/nature08011

    High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat
    journal, June 2013

    • Tian, Xiao; Azpurua, Jorge; Hine, Christopher
    • Nature, Vol. 499, Issue 7458
    • DOI: 10.1038/nature12234

    Genome analysis reveals insights into physiology and longevity of the Brandt’s bat Myotis brandtii
    journal, August 2013

    • Seim, Inge; Fang, Xiaodong; Xiong, Zhiqiang
    • Nature Communications, Vol. 4, Issue 1
    • DOI: 10.1038/ncomms3212

    Cancer selection
    journal, March 2003

    • Leroi, Armand M.; Koufopanou, Vassiliki; Burt, Austin
    • Nature Reviews Cancer, Vol. 3, Issue 3
    • DOI: 10.1038/nrc1016

    The evolutionary dynamics of cancer prevention
    journal, August 2010

    • Gatenby, Robert A.; Gillies, Robert J.; Brown, Joel S.
    • Nature Reviews Cancer, Vol. 10, Issue 8
    • DOI: 10.1038/nrc2892

    Comparative genetics of longevity and cancer: insights from long-lived rodents
    journal, July 2014

    • Gorbunova, Vera; Seluanov, Andrei; Zhang, Zhengdong
    • Nature Reviews Genetics, Vol. 15, Issue 8
    • DOI: 10.1038/nrg3728

    MAL gene expression in esophageal cancer suppresses motility, invasion and tumorigenicity and enhances apoptosis through the Fas pathway
    journal, May 2003


    Microcomputed tomography colonography for polyp detection in an in vivo mouse tumor model
    journal, February 2005

    • Pickhardt, P. J.; Halberg, R. B.; Taylor, A. J.
    • Proceedings of the National Academy of Sciences, Vol. 102, Issue 9
    • DOI: 10.1073/pnas.0409915102

    Evolution of cooperation among tumor cells
    journal, August 2006

    • Axelrod, R.; Axelrod, D. E.; Pienta, K. J.
    • Proceedings of the National Academy of Sciences, Vol. 103, Issue 36
    • DOI: 10.1073/pnas.0606053103

    Comparative lesion sequencing provides insights into tumor evolution
    journal, March 2008

    • Jones, S.; Chen, W. -d.; Parmigiani, G.
    • Proceedings of the National Academy of Sciences, Vol. 105, Issue 11
    • DOI: 10.1073/pnas.0712345105

    Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat
    journal, October 2009

    • Seluanov, A.; Hine, C.; Azpurua, J.
    • Proceedings of the National Academy of Sciences, Vol. 106, Issue 46
    • DOI: 10.1073/pnas.0905252106

    Investigating stem cells in human colon by using methylation patterns
    journal, August 2001

    • Yatabe, Y.; Tavare, S.; Shibata, D.
    • Proceedings of the National Academy of Sciences, Vol. 98, Issue 19
    • DOI: 10.1073/pnas.191225998

    cDNA cloning and sequence of MAL, a hydrophobic protein associated with human T-cell differentiation.
    journal, April 1987

    • Alonso, M. A.; Weissman, S. M.
    • Proceedings of the National Academy of Sciences, Vol. 84, Issue 7
    • DOI: 10.1073/pnas.84.7.1997

    VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells
    journal, May 1999

    • Cheong, K. H.; Zacchetti, D.; Schneeberger, E. E.
    • Proceedings of the National Academy of Sciences, Vol. 96, Issue 11
    • DOI: 10.1073/pnas.96.11.6241

    Genomic Divergences between Humans and Other Hominoids and the Effective Population Size of the Common Ancestor of Humans and Chimpanzees
    journal, February 2001

    • Chen, Feng-Chi; Li, Wen-Hsiung
    • The American Journal of Human Genetics, Vol. 68, Issue 2
    • DOI: 10.1086/318206

    Spatial structure increases the waiting time for cancer
    journal, November 2011


    'Super p53' mice exhibit enhanced DNA damage response, are tumor resistant and age normally
    journal, November 2002

    • García-Cao, Isabel; García-Cao, Marta; Martín-Caballero, Juan
    • The EMBO Journal, Vol. 21, Issue 22
    • DOI: 10.1093/emboj/cdf595

    Genome and genetic resources from the Cancer Genome Anatomy Project
    journal, April 2001


    CancerGenes: a gene selection resource for cancer genome projects
    journal, January 2007

    • Higgins, M. E.; Claremont, M.; Major, J. E.
    • Nucleic Acids Research, Vol. 35, Issue Database
    • DOI: 10.1093/nar/gkl811

    Lineage selection and the evolution of multistage carcinogenesis
    journal, March 1999

    • Nunney, Leonard
    • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 266, Issue 1418
    • DOI: 10.1098/rspb.1999.0664

    Size, longevity and cancer: age structure
    journal, September 2016

    • Wensink, Maarten J.
    • Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1838
    • DOI: 10.1098/rspb.2016.1510

    Comparative oncology: what dogs and other species can teach us about humans with cancer
    journal, July 2015

    • Schiffman, Joshua D.; Breen, Matthew
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1673
    • DOI: 10.1098/rstb.2014.0231

    Towards cancer-aware life-history modelling
    journal, July 2015

    • Kokko, Hanna; Hochberg, Michael E.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1673
    • DOI: 10.1098/rstb.2014.0234

    Peto's paradox and the hallmarks of cancer: constructing an evolutionary framework for understanding the incidence of cancer
    journal, July 2015

    • Nunney, L.; Muir, B.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1673
    • DOI: 10.1098/rstb.2015.0161

    Using genomic data to unravel the root of the placental mammal phylogeny
    journal, March 2007

    • Murphy, W. J.; Pringle, T. H.; Crider, T. A.
    • Genome Research, Vol. 17, Issue 4
    • DOI: 10.1101/gr.5918807

    Eco‐evolutionary perspectives of the dynamic relationships linking senescence and cancer
    journal, July 2019

    • Lemaître, Jean‐François; Pavard, Samuel; Giraudeau, Mathieu
    • Functional Ecology, Vol. 34, Issue 1
    • DOI: 10.1111/1365-2435.13394

    The real war on cancer: the evolutionary dynamics of cancer suppression
    journal, October 2012


    A database of vertebrate longevity records and their relation to other life‐history traits
    journal, July 2009


    Telomerase activity coevolves with body mass not lifespan
    journal, February 2007


    Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan
    journal, December 2008


    Evolutionary and Biomedical Insights from the Rhesus Macaque Genome
    journal, April 2007


    p53 mutations in human cancers
    journal, July 1991


    The Nature of the Principal Type 1 Interferon-Producing Cells in Human Blood
    journal, June 1999


    The clonal evolution of tumor cell populations
    journal, October 1976


    The null oncogene hypothesis and protection from cancer
    journal, January 2002


    CT Evaluation of the Colon: Inflammatory Disease
    journal, March 2000


    Inactivation of the MAL Gene in Breast Cancer Is a Common Event That Predicts Benefit from Adjuvant Chemotherapy
    journal, February 2009


    A simple algebraic cancer equation: calculating how cancers may arise with normal mutation rates
    journal, January 2010


    Natural resistance to cancers: a Darwinian hypothesis to explain Peto’s paradox
    journal, September 2012


    Epigenetic silencing of MAL, a putative tumor suppressor gene, can contribute to human epithelium cell carcinoma
    journal, January 2010


    Hypermethylated MAL gene – a silent marker of early colon tumorigenesis
    journal, January 2008

    • Lind, Guro E.; Ahlquist, Terje; Kolberg, Matthias
    • Journal of Translational Medicine, Vol. 6, Issue 1
    • DOI: 10.1186/1479-5876-6-13

    Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa
    journal, May 2010


    Cancer in wildlife, a case study: beluga from the St. Lawrence estuary, Québec, Canada.
    journal, March 2002

    • Martineau, Daniel; Lemberger, Karin; Dallaire, André
    • Environmental Health Perspectives, Vol. 110, Issue 3
    • DOI: 10.1289/ehp.02110285

    Marine Mammal Neoplasia: A Review
    journal, November 2006


    Genetic Progression and the Waiting Time to Cancer
    journal, January 2007


    Size, longevity and cancer: age structure
    journal, September 2016

    • Wensink, Maarten J.
    • Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1838
    • DOI: 10.1098/rspb.2016.1510

    Peto's paradox and the promise of comparative oncology
    journal, July 2015

    • Nunney, Leonard; Maley, Carlo C.; Breen, Matthew
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1673
    • DOI: 10.1098/rstb.2014.0177

    Comparative oncology: what dogs and other species can teach us about humans with cancer
    journal, July 2015

    • Schiffman, Joshua D.; Breen, Matthew
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1673
    • DOI: 10.1098/rstb.2014.0231

    Towards cancer-aware life-history modelling
    journal, July 2015

    • Kokko, Hanna; Hochberg, Michael E.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1673
    • DOI: 10.1098/rstb.2014.0234

    Peto's paradox and the hallmarks of cancer: constructing an evolutionary framework for understanding the incidence of cancer
    journal, July 2015

    • Nunney, L.; Muir, B.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1673
    • DOI: 10.1098/rstb.2015.0161

    All's well that ends well: why large species have short telomeres
    journal, January 2018

    • Risques, Rosa Ana; Promislow, Daniel E. L.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 373, Issue 1741
    • DOI: 10.1098/rstb.2016.0448

    Eco‐evolutionary perspectives of the dynamic relationships linking senescence and cancer
    journal, July 2019

    • Lemaître, Jean‐François; Pavard, Samuel; Giraudeau, Mathieu
    • Functional Ecology, Vol. 34, Issue 1
    • DOI: 10.1111/1365-2435.13394

    A mathematical solution to Peto’s paradox using Polya’s urn model: implications for the aetiology of cancer in general
    journal, February 2019


    Divide and conquer: two stem cell populations in squamous epithelia, reserves and the active duty forces
    journal, August 2019

    • Dunaway, Spencer; Rothaus, Alexandra; Zhang, Yuhang
    • International Journal of Oral Science, Vol. 11, Issue 3
    • DOI: 10.1038/s41368-019-0061-2

    Return to the Sea, Get Huge, Beat Cancer: An Analysis of Cetacean Genomes Including an Assembly for the Humpback Whale (Megaptera novaeangliae)
    journal, May 2019

    • Tollis, Marc; Robbins, Jooke; Webb, Andrew E.
    • Molecular Biology and Evolution, Vol. 36, Issue 8
    • DOI: 10.1093/molbev/msz099

    Improving Cancer Drug Discovery by Studying Cancer across the Tree of Life
    journal, November 2019

    • Somarelli, Jason A.; Boddy, Amy M.; Gardner, Heather L.
    • Molecular Biology and Evolution, Vol. 37, Issue 1
    • DOI: 10.1093/molbev/msz254

    From humans to hydra: patterns of cancer across the tree of life: Cancer across the tree of life
    journal, April 2018

    • Albuquerque, Thales A. F.; Drummond do Val, Luisa; Doherty, Aoife
    • Biological Reviews, Vol. 93, Issue 3
    • DOI: 10.1111/brv.12415

    Turning natural adaptations to oncogenic factors into an ally in the war against cancer
    journal, March 2018

    • Vittecoq, Marion; Giraudeau, Mathieu; Sepp, Tuul
    • Evolutionary Applications, Vol. 11, Issue 6
    • DOI: 10.1111/eva.12608