Authors: Jean-Pascal Capp, Frédéric Thomas, Andriy Marusyk, Antoine M. Dujon, Sophie Tissot, Robert Gatenby, Benjamin Roche, Beata Ujvari, James DeGregori, Joel S. Brown, Aurora M. Nedelcu

Source: Evolutionary Applications (Jul 2023)

Abstract

It is traditionally assumed that during cancer development, tumor cells abort their initially cooperative behavior (i.e., cheat) in favor of evolutionary strategies designed solely to enhance their own fitness (i.e., a “selfish” life style) at the expense of that of the multicellular organism. However, the growth and progress of solid tumors can also involve cooperation among these presumed selfish cells (which, by definition, should be noncooperative) and with stromal cells.

The ultimate and proximate reasons behind this paradox are not fully understood. Here, in the light of current theories on the evolution of cooperation, we discuss the possible evolutionary mechanisms that could explain the apparent cooperative behaviors among selfish malignant cells.

In addition to the most classical explanations for cooperation in cancer and in general (by-product mutualism, kin selection, direct reciprocity, indirect reciprocity, network reciprocity, group selection), we propose the idea that “greenbeard” effects are relevant to explaining some cooperative behaviors in cancer.

Also, we discuss the possibility that malignant cooperative cells express or co-opt cooperative traits normally expressed by healthy cells. We provide examples where considerations of these processes could help understand tumorigenesis and metastasis and argue that this framework provides novel insights into cancer biology and potential strategies for cancer prevention and treatment.

The Burrunan dolphins that live in Victoria’s waterways are a unique species. Find out more about this critically endangered mammal in the latest blog post from the Ecological Society of Australia, hosting Grace Day (PhD candidate, The Wild Genes Group, Deakin University).

Listen to Prof Thomas Madsen (Deakin University) explaining how a long-term study of an adder population has provided evidence that polyandry and non-random fertilisation can have positive effects on genetic diversity. Thomas argues that factoring in mating dynamics could help to improve conservation genetic analyses.

Authors: Antoine M. Dujon, Orsolya Vincze, Jean-François Lemaitre, Catherine Alix-Panabières, Pascal Pujol, Mathieu Giraudeau, Beata Ujvari and Frédéric Thomas

Source: Proceedings of the Royal Society B: Biological Sciences (Jun 2023)

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.

Authors: Rodrigo Hamede, Nicholas M. Fountain-Jones, Fernando Arce, Menna Jones, Andrew Storfer, Paul A. Hohenlohe, Hamish McCallum, Benjamin Roche, Beata Ujvari, Frédéric Thomas

Source: Evolutionary Applications (Jun 2023)

Abstract

Infectious diseases are a major threat for biodiversity conservation and can exert strong influence on wildlife population dynamics. Understanding the mechanisms driving infection rates and epidemic outcomes requires empirical data on the evolutionary trajectory of pathogens and host selective processes. Phylodynamics is a robust framework to understand the interaction of pathogen evolutionary processes with epidemiological dynamics, providing a powerful tool to evaluate disease control strategies.

Tasmanian devils have been threatened by a fatal transmissible cancer, devil facial tumour disease (DFTD), for more than two decades. Here we employ a phylodynamic approach using tumour mitochondrial genomes to assess the role of tumour genetic diversity in epidemiological and population dynamics in a devil population subject to 12 years of intensive monitoring, since the beginning of the epidemic outbreak. DFTD molecular clock estimates of disease introduction mirrored observed estimates in the field, and DFTD genetic diversity was positively correlated with estimates of devil population size.

However, prevalence and force of infection were the lowest when devil population size and tumour genetic diversity was the highest. This could be due to either differential virulence or transmissibility in tumour lineages or the development of host defence strategies against infection.

Our results support the view that evolutionary processes and epidemiological trade-offs can drive host-pathogen coexistence, even when disease-induced mortality is extremely high. We highlight the importance of integrating pathogen and population evolutionary interactions to better understand long-term epidemic dynamics and evaluating disease control strategies.

Further reading about this research is available here:

• Tasmanian devil facial tumours reveal secrets of cancer evolution – News and stories by University of Tasmania
• Facial tumours evolve to coexist with Tasmanian devil populations – SCIMEX: Breaking science news for Australia & New zealand

Authors: Margaux Bieuville, Dominique Faugère, Virginie Galibert, Morgane Henard, Antoine M. Dujon, Beata Ujvari, Pascal Pujol, Benjamin Roche and Frédéric Thomas

Source: Frontiers in Ecology and Evolution (Feb 2023)

Abstract

It is increasingly thought that part of human susceptibility to cancer is the result of evolutionary mismatches: our ancestors evolved cancer suppression mechanisms in a world largely different from our modern environments. In that context, it has been shown in cohorts from general Western populations that reproductive traits modulate breast cancer risk.

Overall, the more menses women experience, the more at risk they are to develop postmenopausal breast cancer. This points towards an evolutionary mismatch but brings the question whether the reproductive pattern also modulates the breast cancer risk in menopausal women at high familial risk.

We thus studied the influence of menses on breast cancer risk in a case–control study of 90 postmenopausal women (including BRCA1/2 and non BRCA1/2) nested within a cohort at high familial risk. We tested the association of the lifetime number of menses and the number of menses before first full-term pregnancy with postmenopausal breast cancer risk using Cox survival models.

We showed that the total lifetime number of menses was significantly associated with postmenopausal breast cancer risk and associated with a quicker onset of breast cancer after menopause. Those results align with similar studies lead in general cohorts and suggest that the reproductive pattern modulates the familial risk of developing breast cancer after menopause.

Altogether, those results impact how we envision breast cancer prevention and call for more research on how ecological and genetic factors shape breast cancer risk.

Authors: Thomas Madsen, Jon Loman, Dirk Bauwens, Bo Stille, Håkan Anderberg, Lewis Anderberg, Beata Ujvari

Source: Biological Journal of the Linnean Society (Feb 2023)

Abstract

Climate change has been shown to have significant negative effects on wildlife populations owing to both gradual shifts in mean climatic conditions and an increased frequency of extreme climatic events. Based on a long-term study spanning 40 years, we explore the demographic effect of the exceptionally hot and dry summer of 2018 on the demography of an isolated adder (Vipera berus) population in southern Sweden.

In spring 2019, we observed a dramatic decline in adder relative body mass and a concomitant 50% reduction in population size. Our results strongly suggest that the negative impacts on adder demography were the result of a combination of low prey abundance and adder dehydration caused by the extreme climatic conditions during the previous summer.

The study provides an example of the significant negative effects of ongoing climate change on vertebrate populations and emphasizes the importance of long-term studies to document the demographic effects of extreme climatic events.

Authors: Antoine M Dujon, Aurélie Tasiemski, Pascal Pujol, Anthony Turpin, Beata Ujvari, Frédéric Thomas

Source: Evolution, Medicine, and Public Health (Nov 2022)

Abstract

Why humans historically began to incorporate spices into their diets is still a matter of unresolved debate. For example, a recent study (Bromham et al. 2021, Nat Hum Behav) did not support the most popular hypothesis that spice consumption was a practice favoured by selection in certain environments to reduce food poisoning, parasitic infections, and foodborne diseases.

Because several spices are known to have anticancer effects, we explored, using the same dataset, the hypothesis that natural selection and/or cultural evolution may have favoured spice consumption as an adaptive prophylactic response to reduce the burden of cancerous pathologies.

Patterns of spice use in 36 countries, however, are not consistent with a cancer mitigation mechanism: the age-standardised rate of almost all gastrointestinal cancers was not related to spice consumption. Thus, directions other than foodborne pathogens and cancers should be explored to understand the health reasons, if any, why our ancestors developed a taste for spices.

Authors: Thomas Madsen, Beata Ujvari, Dirk Bauwens, Bernd Gruber, Arthur Georges & Marcel Klaassen

Source: Heredity (Dec 2022)

Abstract

Conservation genetic theory suggests that small and isolated populations should be subject to reduced genetic diversity i.e., heterozygosity and allelic diversity. Our 34 years study of an isolated island population of adders (Vipera berus) in southern Sweden challenges this notion.

Despite a lack of gene flow and a yearly mean estimated reproductive adult population size of only 65 adult adders (range 12–171), the population maintains high levels of heterozygosity and allelic diversity similar to that observed in two mainland populations. Even a 14-year major “bottleneck” i.e., a reduction in adult adder numbers, encompassing at least four adder generations, did not result in any reduction in the island adders’ heterozygosity and allelic diversity. Female adders are polyandrous, and fertilisation is non-random, which our empirical data and modelling suggest are underpinning the maintenance of the population’s high level of heterozygosity.

Our empirical results and subsequent modelling suggest that the positive genetic effects of polyandry in combination with non-random fertilisation, often overlooked in conservation genetic analyses, deserve greater consideration when predicting long-term survival of small and isolated populations.

Authors: Thomas Madsen, Marcel Klaassen, Nynke Raven, Antoine M. Dujon, Geordie Jennings, Frédéric Thomas, Rodrigo Hamede, Beata Ujvari

Source: Molecular Ecology (Oct 2022)

Abstract

A plethora of intrinsic and environmental factors have been shown to influence the length of telomeres, the protector of chromosome ends. Despite the growing interest in infection–telomere interactions, there is very limited knowledge on how transmissible cancers influence telomere maintenance. An emblematic example of transmissible cancer occurs in the Tasmanian devil (Sarcophilus harrisii), whose populations have been dramatically reduced by infectious cancer cells.

To investigate associations between telomere dynamics and the transmissible cancer, we used longitudinal data from a Tasmanian devil population that has been exposed to the disease for over 15 years. We detected substantial temporal variation in individual telomere length (TL), and a positive significant association between TL and age, as well as a marginally significant trend for devils with devil facial tumour disease (DFTD) having longer telomeres. A proportional hazard analysis yielded no significant effect of TL on the development of DFTD.

Like previous studies, we show the complexity that TL dynamics may exhibit across the lifetime of organisms. Our work highlights the importance of long-term longitudinal sampling for understanding the effects of wildlife diseases on TL.