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Cancer and life-history traits: lessons from host–parasite interactions

Published online by Cambridge University Press:  18 February 2016

BEATA UJVARI ,
CHRISTA BECKMANN ,
PETER A. BIRO ,
AUDREY ARNAL ,
AURELIE TASIEMSKI ,
FRANCOIS MASSOL ,
MICHEL SALZET ,
FREDERIC MERY ,
CELINE BOIDIN-WICHLACZ  and
DOROTHEE MISSE
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BEATA UJVARI
Affiliation:
School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University, Geelong, VIC, 3216, Australia
CHRISTA BECKMANN
Affiliation:
School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University, Geelong, VIC, 3216, Australia
PETER A. BIRO
Affiliation:
School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University, Geelong, VIC, 3216, Australia
AUDREY ARNAL
Affiliation:
CREEC/MIVEGEC, UMR IRD/CNRS/UM 5290, 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France
AURELIE TASIEMSKI
Affiliation:
UMR CNRS 8198, Unité Evolution, Ecologie et Paléontologie, Université de Lille1, France
FRANCOIS MASSOL
Affiliation:
UMR CNRS 8198, Unité Evolution, Ecologie et Paléontologie, Université de Lille1, France
MICHEL SALZET
Affiliation:
Laboratoire Protéomique, Réponse Inflammatoire et Spectrométrie de Masse (PRISM) INSERM U1192 – Université Lille, 1-FR 3688, CNRS, France
FREDERIC MERY
Affiliation:
Evolution, Génomes, Comportement & Ecologie, CNRS, IRD, Univ.Paris-Sud, Université Paris Saclay, 91198 Gif-sur-Yvette
CELINE BOIDIN-WICHLACZ
Affiliation:
UMR CNRS 8198, Unité Evolution, Ecologie et Paléontologie, Université de Lille1, France
DOROTHEE MISSE
Affiliation:
CREEC/MIVEGEC, UMR IRD/CNRS/UM 5290, 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France
FRANCOIS RENAUD
Affiliation:
CREEC/MIVEGEC, UMR IRD/CNRS/UM 5290, 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France
MARION VITTECOQ
Affiliation:
Centre de Recherche de la Tour du Valat, le Sambuc, 13200 Arles, France
TAZZIO TISSOT
Affiliation:
CREEC/MIVEGEC, UMR IRD/CNRS/UM 5290, 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France
BENJAMIN ROCHE
Affiliation:
CREEC/MIVEGEC, UMR IRD/CNRS/UM 5290, 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France International Center for Mathematical and Computational Modelling of Complex Systems (UMI IRD/UPMC UMMISCO), 32 Avenue Henri Varagnat, 93143 Bondy Cedex, France
ROBERT POULIN
Affiliation:
Department of Zoology, University of Otago, PO BOX 56, New-Zealand
FREDERIC THOMAS*
Affiliation:
CREEC/MIVEGEC, UMR IRD/CNRS/UM 5290, 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France
*
* Corresponding author. CREEC/ MIVEGEC, UMR IRD/CNRS/UM 5290, 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France. Phone +33 (0)4 67 41 63 18. Fax: +33 (0)4 67 41 63 30. E-mail: Frederic.thomas2@ird.fr
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Summary

Despite important differences between infectious diseases and cancers, tumour development (neoplasia) can nonetheless be closely compared to infectious disease because of the similarity of their effects on the body. On this basis, we predict that many of the life-history (LH) responses observed in the context of host–parasite interactions should also be relevant in the context of cancer. Parasites are thought to affect LH traits of their hosts because of strong selective pressures like direct and indirect mortality effects favouring, for example, early maturation and reproduction. Cancer can similarly also affect LH traits by imposing direct costs and/or indirectly by triggering plastic adjustments and evolutionary responses. Here, we discuss how and why a LH focus is a potentially productive but under-exploited research direction for cancer research, by focusing our attention on similarities between infectious disease and cancer with respect to their effects on LH traits and their evolution. We raise the possibility that LH adjustments can occur in response to cancer via maternal/paternal effects and that these changes can be heritable to (adaptively) modify the LH traits of their offspring. We conclude that LH adjustments can potentially influence the transgenerational persistence of inherited oncogenic mutations in populations.

Keywords

Cancerevolutionary ecologylife-history traitsparasitesplasticity
Type
Review Article
Information
Parasitology , Volume 143 , Issue 5 , April 2016 , pp. 533 - 541
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Adamo, S. (1999). Evidence for adaptive changes in egg laying in crickets exposed to bacteria and parasites. Animal Behaviour 57, 117–124.CrossRefGoogle ScholarPubMed
Aktipis, C. A. and Nesse, R. M. (2013). Evolutionary foundations for cancer biology. Evolutionary Applications 6, 144–159.CrossRefGoogle ScholarPubMed
Balls, M. (1962). Spontaneous neoplasms in amphibia: a review and descriptions of six new cases. Cancer Research 22, 1142e1154.Google ScholarPubMed
Bentvelzen, P., Daams, J. H., Hageman, P. and Calafat, J. (1970). Genetic transmission of viruses that incite mammary tumor in mice. Proceedings of the National Academy of Sciences of the United States of America 67, 377–384.CrossRefGoogle ScholarPubMed
Biro, P. A. and Stamps, J. A. (2008). Are animal personality traits linked to life-history productivity? Trends in Ecology and Evolution 23, 361–368.Google ScholarPubMed
Biro, P. A., Adriaenssens, B. and Sampson, P. (2014). Individual and sex-specific differences in intrinsic growth rate covary with consistent individual differences in behaviour. Journal of Animal Ecology 83, 1186–1195.CrossRefGoogle ScholarPubMed
Bodmer, W. F. (2006). Cancer genetics: colorectal cancer as a model. Journal of Human Genetic 51, 391–396.CrossRefGoogle ScholarPubMed
Boyer, N., Réale, D., Marmet, J., Pisanu, B. and Chapuis, J. L. (2010). Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus . Journal of Animal Ecology 79, 538–547.CrossRefGoogle Scholar
Brill, R. W., Balazs, G. H., Holland, K. N., Chang, R. K. C., Sullivan, S. and George, J. C. (1995). Daily movements, habitat use, and submergence intervals of normal and tumor-bearing juvenile green turtles (Chelonia mydas) within a foraging area in the Hawaiian Islands. Journal of Experimental Marine Biology and Ecology 185, 203e218.CrossRefGoogle Scholar
Bromfield, J. J., Schjenken, J. E., Chin, P. Y., Care, A. S., Jasper, M. J. and Robertson, S. A. (2014). Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proceedings of the National Academy of Sciences of the United States of America 111, 2200–2205.CrossRefGoogle ScholarPubMed
Browning, H. M., Gulland, F. M. D., Hammond, J. A., Colegrove, K. M. and Hall, A. J. (2015). Common cancer in a wild animal: the California sea lion (Zalophus californianus) as an emerging model for carcinogenesis. Philosophical Transactions of the Royal Society B 370, 20140228 Published 8 June 2015.CrossRefGoogle Scholar
Bull, C., Godfrey, S. and Gordon, D. (2012). Social networks and the spread of Salmonella in a sleepy lizard population. Molecular Ecology 21, 4386–4392.CrossRefGoogle Scholar
Caulin, A. F. and Maley, C. C. (2011). Peto's Paradox: evolution's prescription for cancer prevention. Trends in Ecology & Evolution 26, 175–182.CrossRefGoogle ScholarPubMed
Chaloupka, M., Balazs, G. H. and Work, T. M. (2009). Rise and fall over 26 years of a marine epizootic in Hawaiian green sea turtles. Journal of Wildlife Diseases 45, 1138e1142.CrossRefGoogle ScholarPubMed
Chen, X., Chen, J., Wen, J., Xu, C., Zhang, S., Zhou, Y. H. and Hu, Y. (2013). Breastfeeding is not a risk factor for mother-to-child transmission of Hepatitis B Virus. PLoS ONE 8, e55303.CrossRefGoogle Scholar
Ciocan, C. and Sunila, I. (2005). Disseminated neoplasia in blue mussels, Mytilus galloprovincialis, from the Black Sea, Romania. Marine Pollution Bulletin 50, 1335e1339. http://dx.doi.org/10.1016/j.marpolbul.2005.04.042.CrossRefGoogle ScholarPubMed
Ciocan, C. M., Moore, J. D. and Rotchell, J. M. (2006). The role of ras gene in the development of haemic neoplasia in Mytilus trossulus . Marine Environmental Research 62, S147eS150. http://dx.doi.org/10.1016j.marenvres.2006.04.020.CrossRefGoogle ScholarPubMed
Coovadia, H. M., Rollins, N. C., Bland, R. M., Little, K., Coutsdoudis, A., Bennish, M. L. and Newell, M. L. (2007). Mother-to-child transmission of HIV-1 infection during exclusive breastfeeding in the first 6 months of life: an intervention cohort study Lancet 369, 1107–1116.CrossRefGoogle ScholarPubMed
Crean, A. J., Dwyer, J. M. and Marshall, D. J. (2012). Fertilization is not a new beginning: the relationship between sperm longevity and offspring performance. PLoS ONE 7, e49167.CrossRefGoogle Scholar
Crean, A. J., Dwyer, J. M. and Marshall, D. J. (2013). Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology 94, 2575–2582.CrossRefGoogle ScholarPubMed
Débarre, F., Lion, S., van Baalen, M. and Gandon, S. (2012). Evolution of host life-history traits in a spatially structured host–parasite system. The American Naturalist 179, 52–63.CrossRefGoogle Scholar
Domazet-Loso, T., Klimovich, A., Anokhin, B., Anton-Erxleben, F., Hamm, M. J., Lange, C. and Bosch, T. C. G. (2014). Naturally occurring tumours in the basal metazoan Hydra . Nature Communications 5, 1–8.Google ScholarPubMed
d'Offay, J. M., Eberle, R., Sucol, Y., Schoelkopf, L., White, M. A., Valentine, B. D., White, G. L. and Lerche, N. W. (2007). Transmission dynamics of simian T-lymphotropic virus type 1 (STLV1) in a baboon breeding colony: predominance of female-to-female transmission. Comparative Medicine 57, 105–114.Google Scholar
Duesberg, P., Mandrioli, D., McCormack, A. and Nicholson, J. M. (2011). Is carcinogenesis a form of speciation? Cell Cycle 10, 2100–2114.CrossRefGoogle ScholarPubMed
Dunn, J. (2013). Lymphoid Leukosis in Poultry. http://www.merckvetmanual.com/mvm/poultry/neoplasms/lymphoid_leukosis_in_poultry.html Google Scholar
Dunn, J. C., Cole, E. F. and Quinn, J. L. (2011). Personality and parasites: sex-dependent associations between avian malaria infection and multiple behavioural traits. Behavioral Ecology and Sociobiology 65, 1459–1471.CrossRefGoogle Scholar
Easton, D. F., Ford, D. and Bishop, D. T. (1995). Breast and ovarian cancer incidence in BRCA1-mutation carriers. Breast cancer linkage consortium. American Journal of Human Genetics 56, 265–271.Google ScholarPubMed
Ewald, P. W. and Swain Ewald, H. A. (2012). Infection, mutation, and cancer evolution. Journal of Molecular Medicine 90, 535–541.CrossRefGoogle ScholarPubMed
Ewald, P. W. and Swain Ewald, H. A. (2013). Toward a general evolutionary theory of oncogenesis. Evolutionary Applications 6, 70–81.CrossRefGoogle Scholar
Ewald, P. W. and Swain Ewald, H. A. (2014). Joint infectious causation of human cancers. Advances in Parasitology 84, 1–26.CrossRefGoogle ScholarPubMed
Ewald, P. W. and Swain Ewald, H. A. (2015). Infection and cancer in multicellular organisms. Philosophical Transactions of the Royal Society B 370, 1–11.CrossRefGoogle ScholarPubMed
Fleming, J. L., Huang, T. H. and Toland, A. E. (2008). The role of parental and grandparental epigenetic alterations in familial cancer risk. Cancer Research 68, 9116–9121.Google ScholarPubMed
Folkman, J. and Kalluri, R. (2004). Cancer without disease. Nature 427, 787–787.CrossRefGoogle ScholarPubMed
Forbes, M. R. L. (1993). Parasitism and host reproductive effort. Oikos 67, 444–450.CrossRefGoogle Scholar
Fredensborg, B. L. and Poulin, R. (2006). Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. Journal of Animal Ecology 75, 44–53.CrossRefGoogle Scholar
Gallizzi, K., Alloitteau, O., Harrang, E. and Richner, H. (2008). Fleas, parental care, and transgenerational effects on tick load in the great tit. Behavioral Ecology 19, 1225–1234.CrossRefGoogle Scholar
Galimany, E. and Sunila, I. (2008). Several cases of disseminated Neoplasia in Mussels Mytilus edulis (L.) in western long island sound. Journal of Shellfish Research 27, 1201–1207.CrossRefGoogle Scholar
Goyos, A. and Robert, J. (2009). Tumorigenesis and anti-tumor immune responses in Xenopus . Frontiers in Bioscience: A Journal and Virtual Library 14, 167e176.Google ScholarPubMed
Gyimesi, Z. S., Garner, M. M., Burns, R. B., Nichols, D. K., Brannian, R. E., Raymond, J. T. and Nordhausen, R. (2005). High incidence of lymphoid Neoplasia in a colony of Egyptian spiny-tailed lizards (Uromastyx aegyptius). Journal of Zoo and Wildlife Medicine 36, 103–110.CrossRefGoogle Scholar
Hakkarainen, H., Huhta, E., Koskela, E., Mappes, T., Soveri, T. and Suorsa, P. (2007). Eimeria-parasites are associated with a lowered mother's and offspring's body condition in island and mainland populations of the bank vole. Parasitology 134, 23–31.CrossRefGoogle ScholarPubMed
Hart, B. (1994). Behavioural defence against parasites: interaction with parasite invasiveness. Parasitology 109, S139–S151.CrossRefGoogle ScholarPubMed
Hardwick, L. J. A. and Philpott, A. (2015). An oncologis's friend: how Xenopus contributes to cancer research. Developmental Biology 408, 180–187.CrossRefGoogle ScholarPubMed
Hochberg, M. E., Michalakis, Y. and de Meeus, T. (1992). Parasitism as a constraint on the rate of life-history evolution. Journal of Evolutionary Biology 5, 491–504.CrossRefGoogle Scholar
Iritani, R. and Iwasa, Y. (2014). Parasite infection drives the evolution of state-dependent dispersal of the host. Theoretical Population Biology 92, 1–13.CrossRefGoogle ScholarPubMed
Jones, M. E., Cockburn, A., Hamede, R., Hawkins, C., Hesterman, H., Lachish, S., Mann, D., McCallum, H. and Pemberton, D. (2008). Life-history change in disease-ravaged Tasmanian devil populations. Proceedings of the National Academy of Sciences of the United States of America 105, 10023–10027.CrossRefGoogle ScholarPubMed
Kokko, H. and Hochberg, M. E. (2015). Towards cancer-aware life-history modelling. Philosophical Transactions of the Royal Society of London B, Biological Sciences 370, 20140234.Google ScholarPubMed
Lafferty, K. D. (1993). The marine snail, Cerithidea californica, matures at smaller sizes where parasitism is high. Oikos 68, 3–11.Google Scholar
LePage, V., Dutton, C. J., Kummrow, M., McLelland, D. J., Young, K. and Lumsden, J. S. (2012). Neoplasia of captive yellow sea horses (Hippocampus kuda) and weedy sea dragons (Phyllopteryx taeniolatus). Journal of Zoo and Wildlife Medicine 43, 50–58.CrossRefGoogle ScholarPubMed
Mager, D. (2006). Bacteria and cancer: cause, coincidence or cure? A review. Journal of Translational Medicine 4, 14.CrossRefGoogle ScholarPubMed
Martineau, D., Lemberger, K., Dallaire, A., Labelle, P., Lipscomb, T. P., Michel, P. and Mikaelian, I. (2002). Cancer in wildlife, a case study: beluga from the St. Lawrence estuary, Quebec, Canada. Environmental Health Perspectives 110, 285.CrossRefGoogle Scholar
McAloose, D. and Newton, A. L. (2009). Wildlife cancer: a conservation perspective. Nature Reviews Cancer 9, 517–526.CrossRefGoogle Scholar
McCallum, H., Tompkins, D. M., Jones, M., Lachish, S., Marvanek, S., Lazenby, B., Hocking, G., Wiersma, J. and Hawkins, C. E. (2007). Distribution and impacts of tasmanian devil facial tumour disease. Ecohealth 4, 318–325.CrossRefGoogle Scholar
Merlo, L. M. F., Pepper, J. W., Reid, B. J. and Maley, C. C. (2006). Cancer as an evolutionary and ecological process. Nature Reviews Cancer 6, 924–935.CrossRefGoogle ScholarPubMed
Metzger, M. J., Reinisch, C., Sherry, J. and Goff, S. P. (2015). Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams. Cell 161, 255–263.CrossRefGoogle ScholarPubMed
Michalakis, Y. (2009). Parasitism and the evolution of life-history traits. In Ecology and Evolution of Parasitism (ed. Thomas, F., Guégan, J.-F. and F. R.), pp. 19–30. Oxford University Press, New York.Google Scholar
Michalakis, Y. and Hochberg, M. E. (1994). Parasitic effects on host life-history traits: a review of recent studies. Parasite 1, 291–294.CrossRefGoogle ScholarPubMed
Minchella, D. and Loverde, P. (1981). A cost of increased early reproductive effort in the snail Biomphalaria glabrata . American Naturalist 118, 876–881.CrossRefGoogle Scholar
Molyneux, E. M., Rochford, R., Griffin, B., Newton, R., Jackson, G., Menon, G., Harrison, C. J., Israels, T. and Bailey, S. (2012). Burkitt's lymphoma. Lancet 379, 1234–1244.CrossRefGoogle ScholarPubMed
Mostafa, M. H., Sheweita, S. A. and O'Connor, P. J. (1999). Relationship between Schistosomiasis and Bladder Cancer. Clinical Microbiology Reviews 12, 97–111.CrossRefGoogle ScholarPubMed
Moriarty, M. E., Vickers, T. W., Clifford, D. L., Garcelon, D. K., Gaffney, P. M., Lee, K. W., King, J. L., Duncan, C. L. and Boyce, W. M. (2015). Ear mite removal in the Santa Catalina Island Fox (Urocyon littoralis catalinae): controlling risk factors for cancer development. PLoS ONE 10, e0144271.CrossRefGoogle Scholar
Mousseau, T. A., Uller, T., Wapstra, E. and Badyaev, A. V. (2009). Evolution of maternal effects: past and present. Philosophical Transactions of the Royal Society of London B, Biological Sciences 364, 1035–1038.CrossRefGoogle ScholarPubMed
Nunney, L. (2013). The real war on cancer: the evolutionary dynamics of cancer suppression. Evolutionary Applications 6, 11–19.CrossRefGoogle ScholarPubMed
O'Neil, L. L., Burkhard, M. J., Diehl, L. J. and Hoover, E. A. (1995). Vertical transmission of feline immunodeficiency virus. AIDS Research and Human Retroviruses 11, 171–182.CrossRefGoogle ScholarPubMed
Page-Karjian, A., Norton, T. M., Krimer, P., Groner, M., Nelson, S. E. Jr. and Gottdenker, N. L. (2014). Factors influencing survivorship of rehabilitating green sea turtles (Chelonia mydas) with fibropapillomatosis. Journal of Zoo and Wildlife Medicine 45, 507–519.CrossRefGoogle ScholarPubMed
Parrish, S. W. K., Brown, A. E., Chanbancherd, P., Gettayacamin, M. and Parrish, J. H. (2004). Transmission of STLV in a closed colony of macaques. American Journal of Primatology 63, 103–109.CrossRefGoogle Scholar
Polak, M. and Starmer, W. T. (1998). Parasite-induced risk of mortality elevates reproductive effort in male Drosophila. Proceedings Biological Sciences/The Royal Society 265, 2197–2201.Google ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton.CrossRefGoogle Scholar
Poulin, R. and Thomas, F. (2008). Epigenetic effects of infection on the phenotype of host offspring: parasites reaching across host generations. Oikos 117, 331–335.CrossRefGoogle Scholar
Rando, O. J. (2012). Daddy issues: paternal effects on phenotype. Cell 151, 702–708.CrossRefGoogle ScholarPubMed
Reznick, D., Nunney, L. and Tessier, A. (2000). Big houses, big cars, superfleas and the costs of reproduction. Trends in Ecology and Evolution 15, 421–425.CrossRefGoogle ScholarPubMed
Risch, H. A., McLaughlin, J. R., Cole, D. E. C., Rosen, B., Bradley, L., Fan, I., Tang, J., Li, S., Zhang, S., Shaw, P. A. and Narod, S. A. (2006). Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: a kin-cohort study in Ontario, Canada. Journal of the National Cancer Institute 98, 1694–1706.CrossRefGoogle ScholarPubMed
Roche, B., Hochberg, M. E., Caulin, A. F., Maley, C. C., Gatenby, R. A., Missé, D. and Thomas, F. (2012). Natural resistance to cancers: a Darwinian hypothesis to explain Peto's paradox. BMC Cancer 12, 387.CrossRefGoogle ScholarPubMed
Rozhok, A. I. and DeGregori, J. (2015). Toward an evolutionary model of cancer: considering the mechanisms that govern the fate of somatic mutations. Proceedings of the National Academy of Sciences of the United States of America 112, 8914–8921.CrossRefGoogle ScholarPubMed
Ryan, J. L., Carroll, J. K., Ryan, E. P., Mustian, K. M., Fiscella, K. and Morrow, G. R. (2007). Mechanisms of cancer-related fatigue. The Oncologist 12 (Suppl. 1), 22–34.CrossRefGoogle ScholarPubMed
Salomon, R. N. and Jackson, F. R. (2008). Tumors of testis and midgut in aging flies. Fly 2, 265e268.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P. (2011). Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. Oxford University Press, Oxford.Google Scholar
Shimonohara, N., Holland, C. H., Lin, T.-L. and Wigle, W. L. (2012). Naturally occurring neoplasms in pigeons in a research colony: a retrospective study. Avian Diseases 57, 133e139. http://dx.doi.org/10.1637/10244-051012-Case.1.Google Scholar
Seaman, B. and Briffa, M. (2015). Parasites and personality in periwinkles (Littorina littorea): infection status is associated with mean-level boldness but not repeatability. Behavioural Processes 115, 132–134.CrossRefGoogle Scholar
Smith, K. R., Hanson, H. A., Mineau, G. P. and Buys, S. S. (2012). Effects of BRCA1 and BRCA2 mutations on female fertility. Proceedings of the Royal Society B, Biological Sciences 279, 1389–1395.CrossRefGoogle ScholarPubMed
Sorci, G. and Clobert, J. (1995). Effects of maternal parasite load on offspring life-history traits in the common lizard (Lacerta vivipara). Journal of Evolutionary Biology 8, 711–723.CrossRefGoogle Scholar
Sorci, G., Clobert, J. and Michalakis, Y. (1996). Cost of reproduction and cost of parasitism in the common lizard, Lacerta vivipara . Oikos 76, 121–130.CrossRefGoogle Scholar
Sorci, G., Boulinier, T., Gauthier-Clerc, M. and Faivre, B. (2009). The evolutionary ecology of the immune response. In Ecology and Evolution of Parasitism (ed. by Thomas, F., Guégan, J.F., and Renaud, F.), pp. 5–17. Oxford University Press, Oxford.Google Scholar
Sweet, M., Kirkham, N., Bendall, M., Currey, L., Bythell, J. and Heupel, M. (2012). Evidence of melanoma in wild marine fish populations. PLoS ONE 7, e41989.CrossRefGoogle ScholarPubMed
Thomas, F., Guégan, J., Michalakis, Y. and Renaud, F. (2000). Parasites and host life-history traits: implications for community ecology and species co-existence. International Journal for Parasitology 30, 669–674.CrossRefGoogle ScholarPubMed
Thomas, F., Guégan, J.-F. and Renaud, F. (2009). Ecology and Evolution of Parasitism. Oxford University Press.Google Scholar
Thomas, F., Fisher, D., Fort, P., Marie, J.-P., Daoust, S., Roche, B., Grunau, C., Cosseau, C., Mitta, G., Baghdiguian, S., Rousset, F., Lassus, P., Assenat, E., Grégoire, D., Missé, D., Lorz, A., Billy, F., Vainchenker, W., Delhommeau, F., Koscielny, S., Itzykson, R., Tang, R., Fava, F., Ballesta, A., Lepoutre, T., Krasinska, L., Dulic, V., Raynaud, P., Blache, P., Quittau-Prevostel, C. et al. (2013). Applying ecological and evolutionary theory to cancer: a long and winding road. Evolutionary Applications 6, 1–10.CrossRefGoogle Scholar
van Noordwijk, A. J. and de Jong, G. (1986). Acquisition and allocation of resources: their influence on variation in life history tactics. The American Naturalist 128, 137–142.CrossRefGoogle Scholar
Vézilier, J., Nicot, A., Gandon, S. and Rivero, A. (2015). Plasmodium infection brings forward mosquito oviposition. Biology Letters 11(3), 20140840. doi: 10.1098/rsbl.2014.0840.CrossRefGoogle ScholarPubMed
Vickers, T. W., Clifford, D. L., Garcelon, D. K., King, J. L., Duncan, C. L., Gaffney, P. M. and Boyce, W. M. (2015). Pathology and epidemiology of ceruminous gland tumors among endangered Santa Catalina Island foxes (Urocyon littoralis catalinae) in the Channel Islands, USA. PLoS ONE 10, e0143211.CrossRefGoogle Scholar
Vittecoq, M., Roche, B., Daoust, S. P., Ducasse, H., Missé, D., Abadie, J., Labrut, S., Renaud, F., Gauthier-Clerc, M. and Thomas, F. (2013). Cancer: a missing link in ecosystem functioning? Trends in Ecology and Evolution 28, 628–635.CrossRefGoogle Scholar
Vittecoq, M., Ducasse, H., Arnal, A., Møller, A. P., Ujvari, B., Jacqueline, C. B., Tissot, T., Missé, D., Bernex, F., Pirot, N., Lemberger, K., Abadie, J., Labrut, S., Bonhomme, F., Renaud, F., Roche, B. and Thomas, F. (2015). Animal behaviour and cancer. Animal Behaviour 101, 19–26.CrossRefGoogle Scholar
Wagner, L. I. and Cella, D. (2004). Fatigue and cancer: causes, prevalence and treatment approaches. British Journal of Cancer 91, 822–828.CrossRefGoogle ScholarPubMed
Wolf, J. B. and Wade, M. J. (2009). What are maternal effects (and what are they not)? Philosophical Transactions of the Royal Society of London B, Biological Sciences 364, 1107–1115.CrossRefGoogle Scholar
Zajitschek, S., Hotzy, C., Zajitschek, F. and Immler, S. (2014). Short-term variation in sperm competition causes sperm-mediated epigenetic effects on early offspring performance in the zebrafish. Proceedings of the Royal Society of Sciences B 281, 20140422.CrossRefGoogle ScholarPubMed