The effect of placentation type, litter size, lactation and gestation length on cancer risk in mammals

Author:

Dujon Antoine M.12ORCID,Vincze Orsolya34,Lemaitre Jean-François5ORCID,Alix-Panabières Catherine26ORCID,Pujol Pascal27,Giraudeau Mathieu8ORCID,Ujvari Beata12ORCID,Thomas Frédéric2ORCID

Affiliation:

1. Geelong, School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University, Waurn Ponds, Victoria 3216, Australia

2. CREEC/CANECEV (CREES), MIVEGEC, IRD 224–CNRS 5290–Université de Montpellier, Montpellier, France

3. Institute of Aquatic Ecology, Centre for Ecological Research, Debrecen, Hungary

4. Evolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babes-Bolyai University, Cluj-Napoca, Romania

5. CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, Villeurbanne, France

6. Laboratory of Rare Human Circulating Cells (LCCRH), University Hospital of Montpellier, Montpellier, France

7. Centre Hospitalier Universitaire Arnaud de Villeneuve, Montpellier, France

8. Littoral Environnement Et Sociétés (LIENSs), UMR 7266,CNRS- La Rochelle Université, La Rochelle, France

Abstract

Reproduction is a central activity for all living organisms but is also associated with a diversity of costs that are detrimental for survival. Until recently, the cost of cancer as a selective force has been poorly considered. Considering 191 mammal species, we found cancer mortality was more likely to be detected in species having large, rather than low, litter sizes and long lactation lengths regardless of the placentation types. However, increasing litter size and gestation length are not per se associated with an enhanced cancer mortality risk. Contrary to basic theoretical expectations, the species with the highest cancer mortality were not those with the most invasive (i.e. haemochorial) placentation, but those with a moderately invasive (i.e. endotheliochorial) one. Overall, these results suggest that (i) high reproductive efforts favour oncogenic processes' dynamics, presumably because of trade-offs between allocation in reproduction effort and anti-cancer defences, (ii) cancer defence mechanisms in animals are most often adjusted to align reproductive lifespan, and (iii) malignant cells co-opt existing molecular and physiological pathways for placentation, but species with the most invasive placentation have also selected for potent barriers against lethal cancers. This work suggests that the logic of Peto's paradox seems to be applicable to other traits that promote tumorigenesis.

Funder

MAVA Foundation

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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