Lifetime cancer prevalence and life history traits in mammals.

Peto's Paradox cancer comparative oncology life history theory mammals

Journal

Evolution, medicine, and public health
ISSN: 2050-6201
Titre abrégé: Evol Med Public Health
Pays: England
ID NLM: 101616698

Informations de publication

Date de publication:
2020
Historique:
received: 23 12 2019
accepted: 19 05 2020
entrez: 19 11 2020
pubmed: 20 11 2020
medline: 20 11 2020
Statut: epublish

Résumé

Cancer is a common diagnosis in many mammalian species, yet they vary in their vulnerability to cancer. The factors driving this variation are unknown, but life history theory offers potential explanations to why cancer defense mechanisms are not equal across species. Here we report the prevalence of neoplasia and malignancy in 37 mammalian species, representing 11 mammalian orders, using 42 years of well curated necropsy data from the San Diego Zoo and San Diego Zoo Safari Park. We collected data on life history components of these species and tested for associations between life history traits and both neoplasia and malignancy, while controlling for phylogenetic history. These results support Peto's paradox, in that we find no association between lifespan and/or body mass and the prevalence of neoplasia or malignancy. However, a positive relationship exists between litter size and prevalence of malignancy (P = 0.005, Adj. R2 = 0.212), suggesting that a species' life history strategy may influence cancer vulnerabilities. Lastly, we tested for the relationship between placental invasiveness and malignancy. We find no evidence for an association between placental depth and malignancy prevalence (P = 0.618, Adj. R2 = 0.068). Life history theory offers a powerful framework to understand variation in cancer defenses across the tree of life. These findings provide insight into the relationship between life history traits and cancer vulnerabilities, which suggest a trade-off between reproduction and cancer defenses. Why are some mammals more vulnerable to cancer than others? We test whether life history trade-offs may explain this variation in cancer risk. Bigger, longer-lived animals do not develop more cancer compared to smaller, shorter-lived animals. However, we find a positive association between litter size and cancer prevalence in mammals.

Sections du résumé

BACKGROUND BACKGROUND
Cancer is a common diagnosis in many mammalian species, yet they vary in their vulnerability to cancer. The factors driving this variation are unknown, but life history theory offers potential explanations to why cancer defense mechanisms are not equal across species.
METHODOLOGY METHODS
Here we report the prevalence of neoplasia and malignancy in 37 mammalian species, representing 11 mammalian orders, using 42 years of well curated necropsy data from the San Diego Zoo and San Diego Zoo Safari Park. We collected data on life history components of these species and tested for associations between life history traits and both neoplasia and malignancy, while controlling for phylogenetic history.
RESULTS RESULTS
These results support Peto's paradox, in that we find no association between lifespan and/or body mass and the prevalence of neoplasia or malignancy. However, a positive relationship exists between litter size and prevalence of malignancy (P = 0.005, Adj. R2 = 0.212), suggesting that a species' life history strategy may influence cancer vulnerabilities. Lastly, we tested for the relationship between placental invasiveness and malignancy. We find no evidence for an association between placental depth and malignancy prevalence (P = 0.618, Adj. R2 = 0.068).
CONCLUSIONS CONCLUSIONS
Life history theory offers a powerful framework to understand variation in cancer defenses across the tree of life. These findings provide insight into the relationship between life history traits and cancer vulnerabilities, which suggest a trade-off between reproduction and cancer defenses.
LAY SUMMARY BACKGROUND
Why are some mammals more vulnerable to cancer than others? We test whether life history trade-offs may explain this variation in cancer risk. Bigger, longer-lived animals do not develop more cancer compared to smaller, shorter-lived animals. However, we find a positive association between litter size and cancer prevalence in mammals.

Identifiants

pubmed: 33209304
doi: 10.1093/emph/eoaa015
pii: eoaa015
pmc: PMC7652303
doi:

Types de publication

Journal Article

Langues

eng

Pagination

187-195

Subventions

Organisme : NCI NIH HHS
ID : U54 CA217376
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA185138
Pays : United States
Organisme : NCI NIH HHS
ID : U2C CA233254
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA091955
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA170595
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA140657
Pays : United States

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Foundation for Evolution, Medicine, and Public Health.

Références

JAMA. 2016 Apr 26;315(16):1789
pubmed: 27115385
Vet Clin North Am Exot Anim Pract. 2017 Jan;20(1):183-208
pubmed: 27890288
J Med Microbiol. 2019 Jul;68(7):1072-1080
pubmed: 31162024
Am Nat. 2002 Dec;160(6):712-26
pubmed: 18707460
Philos Trans R Soc Lond B Biol Sci. 2015 Jul 19;370(1673):
pubmed: 26056356
Nat Rev Cancer. 2018 Oct;18(10):646-661
pubmed: 30116020
Philos Trans R Soc Lond B Biol Sci. 2015 Jul 19;370(1673):
pubmed: 26056366
Nature. 2013 Jul 18;499(7458):346-9
pubmed: 23783513
Vet Pathol. 2016 May;53(3):691-6
pubmed: 26846576
Mol Biol Rep. 2018 Feb;45(1):63-69
pubmed: 29288425
Cancer Cell. 2018 Apr 9;33(4):607-619.e15
pubmed: 29634948
Nat Rev Cancer. 2018 Jul;18(7):433-441
pubmed: 29622806
PLoS One. 2015 Jul 13;10(7):e0132563
pubmed: 26168031
J Evol Biol. 2008 Nov;21(6):1763-78
pubmed: 18808441
Evol Med Public Health. 2014 Oct 15;2014(1):136-45
pubmed: 25324490
J Zoo Wildl Med. 2017 Jun;48(2):394-403
pubmed: 28749282
Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3203-8
pubmed: 16492730
Nature. 2007 Mar 29;446(7135):507-12
pubmed: 17392779
Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11547-52
pubmed: 23798387
Int J Breast Cancer. 2012;2012:654698
pubmed: 22295247
Mol Biol Evol. 2020 Jan 1;37(1):11-17
pubmed: 31688937
J Comp Pathol. 2002 Feb-Apr;126(2-3):226-30
pubmed: 11945013
JAMA. 2015 Nov 3;314(17):1850-60
pubmed: 26447779
J Comp Pathol. 2012 Aug-Oct;147(2-3):368-75
pubmed: 22424809
Proc Natl Acad Sci U S A. 2012 Nov 20;109(47):19392-6
pubmed: 23129611
J Natl Cancer Inst. 1977 Jul;59(1):185-98
pubmed: 577508
Philos Trans R Soc Lond B Biol Sci. 2015 Jul 19;370(1673):
pubmed: 26056372
Front Endocrinol (Lausanne). 2017 Aug 04;8:187
pubmed: 28824547
Am Nat. 2011 Jan;177(1):86-98
pubmed: 21087154
J Evol Biol. 2009 Aug;22(8):1770-4
pubmed: 19522730
J Zoo Wildl Med. 1999 Jun;30(2):268-72
pubmed: 10484144
Sci Rep. 2016 Nov 07;6:36361
pubmed: 27819303
Philos Trans R Soc Lond B Biol Sci. 2015 Mar 5;370(1663):20140072
pubmed: 25602076
Mol Biol Evol. 2020 Feb 1;37(2):320-326
pubmed: 31642480
BMC Cancer. 2012 Sep 03;12:387
pubmed: 22943484
Philos Trans R Soc Lond B Biol Sci. 2015 Jul 19;370(1673):
pubmed: 26056359
Placenta. 2009 Nov;30(11):949-67
pubmed: 19800685
Philos Trans R Soc Lond B Biol Sci. 2015 Jul 19;370(1673):
pubmed: 26056362
Q Rev Biol. 1993 Dec;68(4):495-532
pubmed: 8115596
Philos Trans R Soc Lond B Biol Sci. 2015 Jul 19;370(1673):
pubmed: 26056364
Biol Rev Camb Philos Soc. 2018 Aug;93(3):1715-1734
pubmed: 29663630
BMC Biol. 2017 Jul 13;15(1):60
pubmed: 28705195
Placenta. 2012 Oct;33(10):763-8
pubmed: 22840298
Proc Natl Acad Sci U S A. 2013 May 7;110(19):7760-5
pubmed: 23610401
Science. 1981 May 1;212(4494):571-3
pubmed: 7209555
F1000Res. 2017 Dec 7;6:2109
pubmed: 29259779
Philos Trans R Soc Lond B Biol Sci. 2015 Jul 19;370(1673):
pubmed: 26056363
Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):201-5
pubmed: 8552604

Auteurs

Amy M Boddy (AM)

Department of Anthropology, University of California, Santa Barbara, CA, USA.

Lisa M Abegglen (LM)

Department of Pediatrics and Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA.

Allan P Pessier (AP)

Washington Animal Disease Diagnostic Laboratory, Washington State University, Pullman, WA, USA.

Athena Aktipis (A)

Department of Psychology, Arizona State University, Tempe, AZ.
Arizona Cancer Evolution Center, Biodesign Institute, Arizona State University, Tempe, AZ, USA.

Joshua D Schiffman (JD)

Department of Pediatrics and Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA.

Carlo C Maley (CC)

Arizona Cancer Evolution Center, Biodesign Institute, Arizona State University, Tempe, AZ, USA.

Carmel Witte (C)

Institute for Conservation Research, San Diego Zoo Global, CA, USA.

Classifications MeSH