Authors: Hiske Klaassen, Sophie Tissot, Jordan Meliani, Justine Boutry, Anna Miltiadous, Peter A. Biro, David J. Mitchell, Beata Ujvari, Aaron Schultz, Frédéric Thomas and Antoine M. Dujon

Source: Proceedings of the Royal Society B (Feb 2024)

Abstract

Wildlife is increasingly exposed to sublethal transient cancer risk factors, including mutagenic substances, which activates their anti-cancer defences, promotes tumourigenesis, and may negatively impact populations. Little is known about how exposure to cancer risk factors impacts the behaviour of wildlife.

Here, we investigated the effects of a sublethal, short-term exposure to a carcinogen at environmentally relevant concentrations on the activity patterns of wild Girardia tigrina planaria during a two-phase experiment, consisting of a 7-day exposure to cadmium period followed by a 7-day recovery period. To comprehensively explore the effects of the exposure on activity patterns, we employed the double hierarchical generalized linear model framework which explicitly models residual intraindividual variability in addition to the mean and variance of the population.

We found that exposed planaria were less active compared to unexposed individuals and were able to recover to pre-exposure activity levels albeit with a reduced variance in activity at the start of the recovery phase. Planaria showing high activity levels were less predictable with larger daily activity variations and higher residual variance. Thus, the shift in behavioural variability induced by an exposure to a cancer risk factor can be quantified using advanced tools from the field of behavioural ecology. This is required to understand how tumourous processes affect the ecology of species.

Authors: Georgina Bramwell, Aaron G. Schultz, Geordie Jennings, Urmi Nishat Nini, Caitlin Vanbeek, Peter A. Biro, Christa Beckmann, Antoine M. Dujon, Frédéric Thomas, Craig D.H. Sherman, Beata Ujvari

Source: Science of The Total Environment (Dec 2023)

Abstract

The presence of doubly uniparental inheritance (DUI) in bivalves represents a unique mode of mitochondrial transmission, whereby paternal (male-transmitted M-type) and maternal (female-transmitted F-type) haplotypes are transmitted to offspring separately. Male embryos retain both haplotypes, but the M-type is selectively removed from females.

Due to the presence of heteroplasmy in males, mtDNA can recombine resulting in a ‘masculinized’ haplotype referred to as M^f-type. While mtDNA recombination is usually rare, it has been recorded in multiple mussel species across the Northern Hemisphere. Given that mitochondria are the powerhouse of the cell, different mtDNA haplotypes may have different selective advantages under diverse environmental conditions. This may be particularly important for sperm fitness and fertilization success. In this study we aimed to i) determine the presence, prevalence of the M^f-type in Australian blue mussels (Mytilus sp.) and ii) investigate the effect of M^f-mtDNA on sperm performance (a fitness correlate).

We found a high prevalence of recombined mtDNA (≈35 %) located within the control region of the mitochondrial genome, which occurred only in specimens that contained Southern Hemisphere mtDNA. The presence of two female mitotypes were identified in the studied mussels, one likely originating from the Northern Hemisphere, and the other either representing the endemic M. planulatus species or introduced genotypes from the Southern Hemisphere. Despite having recombination events present in a third of the studied population, analysis of sperm performance indicated no difference in fertilization success related to mitotype.

Authors: Georgina Bramwell, Aaron G. Schultz, Thomas Madsen, Frédéric Thomas, Nick Macdonald, Antoine M. Dujon, Craig D.H. Sherman, Beata Ujvari

Source: Aquaculture (Sep 2023)

Abstract

As valuable ecosystem engineers, blue mussels, are one of the most ecologically and economically important bivalve species in Australia. The need for understanding levels of genetic diversity in both wild and farmed populations of Australian mussels is ever-growing due to the increased risk of disease and decreased fitness associated with the constantly changing global environment.

This study, therefore, investigated the phylogenetic relationship, and the genetic variation of farmed blue mussels (Mytilus sp., previously noted as M. galloprovincialis, M. planulatus or a hybrid of both) at four sites along the south coast of Australia, Victoria, South Australia, Western Australia, and Tasmania.

Analyses of two genes, Cytochrome c oxidase subunit 1 gene (mtCOI) and the nuclear gene Elongation factor 1 alpha (EF1a) was completed for all mussels sampled. The phylogenetic reconstruction of mtDNA sequences was not able to cluster the samples into species. The analyses of the nuclear marker (EF1a) returned similar results, except that we could conclude the Australian samples not being M. chilensis. Furthermore, the analyses of EF1a revealed the presence of hybridisation, a pattern commonly observed in mussels.

The genetic diversity analysis of mtCOI demonstrated that samples from Victoria and Western Australia had the highest genetic diversity, while South Australia had the lowest. When analysing the nuclear EF1a sequences, mussels from Western Australian had the lowest genetic diversity, and the Victorian samples had the highest.

The study extended our knowledge on the population genetic variation of farmed blue mussels (Mytilus sp.) along the south coast of Australia. The identified genetic differences between the four southern states of Australia could be interesting for the aquaculture industry when aiming for more adaptable and profitable stocks.

Authors: Antoine M. Dujon, Jérémy Jeanjean, Orsolya Vincze, Mathieu Giraudeau, Jean-François Lemaître, Pascal Pujol, Beata Ujvari, Frédéric Thomas

Source: Ecology and Evolution (Sep 2023)

Abstract

The hygiene hypothesis, according to which the recent reduction of exposure to infectious agents in the human species would be the origin of various diseases, including autoimmune diseases and cancer, has often been proposed but not properly tested on animals.

Here, we evaluated the relevance of this hypothesis to cancer risk in mammals in an original way, namely by using information on zoo mammals. We predicted that a higher richness of parasitic cohorts in the species’ natural habitat would result in a greater occurrence of evolutionary mismatch due to the reduction of parasites in captive conditions. This, in turn, could contribute to an increased risk of developing lethal cancers.

Using a comparative analysis of 112 mammalian species, we explored the potential relationship between cancer risk and parasite species richness using generalized phylogenetic least squares regressions to relate parasite species richness to cancer risk data.

We found no strong evidence that parasite species richness increased cancer risk in zoo mammals for any of the parasite groups we tested. Without constituting definitive proof of the irrelevance of the hygienic hypothesis, our comparative study using zoo mammals does not support it, at least with respect to cancer risks.

Authors: Badreddine Bererhi, Pierre Duchesne, Tonia S. Schwartz, Beata Ujvari, Erik Wapstra, Mats Olsson

Source: Ecology and Evolution (Mar 2023)

Abstract

The harmful effects of close inbreeding have been recognized for centuries and, with the rise of Mendelian genetics, was realized to be an effect of homozygosis. This historical background led to great interest in ways to quantify inbreeding, its depression effects on the phenotype and flow-on effects on mate choice and other aspects of behavioral ecology.

The mechanisms and cues used to avoid inbreeding are varied and include major histocompatibility complex (MHC) molecules and the peptides they transport as predictors of the degree of genetic relatedness.

Here, we revisit and complement data from a Swedish population of sand lizards (Lacerta agilis) showing signs of inbreeding depression to assess the effects of genetic relatedness on pair formation in the wild. Parental pairs were less similar at the MHC than expected under random mating but mated at random with respect to microsatellite relatedness. MHC clustered in groups of RFLP bands but no partner preference was observed with respect to partner MHC cluster genotype. Male MHC band patterns were unrelated to their fertilization success in clutches selected for analysis on the basis of showing mixed paternity.

Thus, our data suggest that MHC plays a role in pre-copulatory, but not post-copulatory partner association, suggesting that MHC is not the driver of fertilization bias and gamete recognition in sand lizards.

Authors: Justine Boutry, Marie Buysse, Sophie Tissot, Chantal Cazevielle, Rodrigo Hamede, Antoine M. Dujon, Beata Ujvari, Mathieu Giraudeau, Alexander Klimovich, Frédéric Thomas & Jácint Tökölyi

Source: Scientific Reports (May 2023)

Abstract

Hydras are freshwater cnidarians widely used as a biological model to study different questions such as senescence or phenotypic plasticity but also tumoral development. The spontaneous tumors found in these organisms have been so far described in two female lab strains domesticated years ago (Hydra oligactis and Pelmatohydra robusta) and the extent to which these tumors can be representative of tumors within the diversity of wild hydras is completely unknown.

In this study, we examined individuals isolated from recently sampled wild strains of different sex and geographical origin, which have developed outgrowths looking like tumors. These tumefactions have common features with the tumors previously described in lab strains: are composed of an accumulation of abnormal cells, resulting in a similar enlargement of the tissue layers. However, we also found diversity within these new types of tumors. Indeed, not only females, but also males seem prone to form these tumors. Finally, the microbiota associated to these tumors is different from the one involved in the previous lineages exhibiting tumors. We found that tumorous individuals hosted yet undescribed Chlamydiales vacuoles.

This study brings new insights into the understanding of tumor susceptibility and diversity in brown hydras from different origins.

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.