scholarly journals Transmissible cancers and the evolution of sex under the Red Queen hypothesis

2020 ◽  
Author(s):  
Thomas G. Aubier ◽  
Matthias Galipaud ◽  
E. Yagmur Erten ◽  
Hanna Kokko

AbstractThe predominance of sexual reproduction in eukaryotes remains paradoxical in evolutionary theory. Of the hypotheses proposed to resolve this paradox, the “Red Queen hypothesis” emphasizes the potential of antagonistic interactions to cause fluctuating selection, which favours the evolution and maintenance of sex. While empirical and theoretical developments have focused on host-parasite interactions, the premises of the Red Queen theory apply equally well to any type of antagonistic interactions. Recently, it has been suggested that early multicellular organisms with basic anticancer defenses were presumably plagued by antagonistic interactions with transmissible cancers, and that this could have played a pivotal role in the evolution of sex. Here, we dissect this argument using a population genetic model. One fundamental aspect distinguishing transmissible cancers from other parasites is the continual production of cancerous cell lines from hosts’ own tissues. We show that this influx dampens fluctuating selection and therefore makes the evolution of sex more difficult than in standard Red Queen models. Although coevolutionary cycling can remain sufficient to select for sex under some parameter regions of our model, we show that the size of those regions shrinks once we account for epidemiological constraints. Altogether, our results suggest that horizontal transmission of cancerous cells is unlikely to cause fluctuating selection favouring sexual reproduction. Nonetheless, we confirm that vertical transmission of cancerous cells can promote the evolution of sex through a separate mechanism, known as similarity selection, that does not depend on coevolutionary fluctuations.

PLoS Biology ◽  
2020 ◽  
Vol 18 (11) ◽  
pp. e3000916
Author(s):  
Thomas G. Aubier ◽  
Matthias Galipaud ◽  
E. Yagmur Erten ◽  
Hanna Kokko

The predominance of sexual reproduction in eukaryotes remains paradoxical in evolutionary theory. Of the hypotheses proposed to resolve this paradox, the ‘Red Queen hypothesis’ emphasises the potential of antagonistic interactions to cause fluctuating selection, which favours the evolution and maintenance of sex. Whereas empirical and theoretical developments have focused on host-parasite interactions, the premises of the Red Queen theory apply equally well to any type of antagonistic interactions. Recently, it has been suggested that early multicellular organisms with basic anticancer defences were presumably plagued by antagonistic interactions with transmissible cancers and that this could have played a pivotal role in the evolution of sex. Here, we dissect this argument using a population genetic model. One fundamental aspect distinguishing transmissible cancers from other parasites is the continual production of cancerous cell lines from hosts’ own tissues. We show that this influx dampens fluctuating selection and therefore makes the evolution of sex more difficult than in standard Red Queen models. Although coevolutionary cycling can remain sufficient to select for sex under some parameter regions of our model, we show that the size of those regions shrinks once we account for epidemiological constraints. Altogether, our results suggest that horizontal transmission of cancerous cells is unlikely to cause fluctuating selection favouring sexual reproduction. Nonetheless, we confirm that vertical transmission of cancerous cells can promote the evolution of sex through a separate mechanism, known as similarity selection, that does not depend on coevolutionary fluctuations.


2015 ◽  
Vol 1 (1) ◽  
pp. 36
Author(s):  
Samantha A. Klosak

Sexual reproduction is a very costly process: the growth rate of asexual lineages exceeds that of sexual lineages. Nonetheless, sex is prevalent in nature. The Red Queen Hypothesis argues that, because sex and recombination generate genetically variable offspring that may escape infection by coevolving parasites, parasites select for sex in hosts (Lively & Dybdahl, 2000). Our research directly tests if the Red Queen can explain the maintenance of sex in a natural population. This experiment focuses on a natural population of the snail Potamopyrgus antipodarum, which is native to New Zealand. Individuals of this species are either diploid and sexually reproducing or triploid and asexually reproducing (Lively & Osnas, 2006). This snail is naturally infected by the trematode parasite, Microphallus, which is sterilizing and thus exerts strong selection on its host. The Red Queen Hypothesis predicts that parasites should periodically increase the fitness of sexual relative to asexual individuals. We accordingly established mesocosms containing both sexual and asexual snails from the same natural population. Half of these mesocosms were exposed to parasites and the other half were not. These snails were then allowed to reproduce over the course of a year. We used flow cytometry to determine the frequency of diploids in the parents and the offspring, and thereby the fitness of sexual individuals in the presence and absence of parasites. Interestingly, we find that sexual individuals are currently more susceptible to parasites than are asexual individuals. In tanks in which sexual parents are relatively more infected, the frequency of sexual individuals declined significantly more in the offspring generation, indicating a fitness consequence of parasitism for sexual reproduction. Our findings suggest that parasite selection can indeed operate on reproductive mode. Moreover, our results are consistent with theory (King, Delph, Jokela, & Lively, 2009) and a prior field study in our system indicating that the direction of parasite selection is variable, such that parasites periodically select against sexual reproduction (Vergara, Lively, King, & Jokela, 2013). This current experiment will continue for multiple years in order to track the variation in parasite selection on sex through time. 


2006 ◽  
Vol 84 (6) ◽  
pp. 808-816 ◽  
Author(s):  
J.A. Mee ◽  
L. Rowe

In light of the inherent disadvantages of sexual reproduction, the existence of sex is often seen as a paradox. There are a variety of hypothetical benefits of sexual reproduction that may balance its disadvantages. The Red Queen hypothesis proposes that sexually reproducing species are better able to evolve resistance to parasites than asexually reproducing species. A prediction of the Red Queen hypothesis is that a parasite should evolve to preferentially exploit an asexual species over a sexual species. To test this central prediction of the Red Queen hypothesis, intensity of infection by the parasite Gyrodactylus eos Mayes, 1977 (Monogenea) was compared between sympatric asexual and sexual fish species in the genus Phoxinus Rafinesque, 1820. In each lake where these species coexist, the asexual fish should suffer higher intensities of infection than the sexual fish. In the majority of lakes sampled, there were more parasites on asexual than sexual fish.


2019 ◽  
Author(s):  
Sang Woo Park ◽  
Benjamin M Bolker

AbstractSexual reproduction persists in nature despite its large cost. The Red Queen Hypothesis postulates that parasite pressure maintains sexual reproduction in the host population by selecting for the ability to produce rare genotypes that are resistant to infection. Mathematical models have been used to lay theoretical foundations for the hypothesis; empirical studies have confirmed these predictions. For example, Lively used a simple host-parasite model to predict that the frequency of sexual hosts should be positively correlated with the prevalence of infection. Lively et al. later confirmed the prediction through numerous field studies of snail-trematode systems in New Zealand. In this study, we fit a simple metapopulation host-parasite coevolution model to three data sets, each representing a different snail-trematode system, by matching the observed prevalence of sexual reproduction and trematode infection among hosts. Using the estimated parameters, we perform a power analysis to test the feasibility of observing the positive correlation predicted by Lively. We discuss anomalies in the data that are poorly explained by the model and provide practical guidance to both modelers and empiricists. Overall, our study suggests that a simple Red Queen model can only partially explain the observed relationships between parasite infection and the maintenance of sexual reproduction.


2020 ◽  
Author(s):  
Ben Ashby

AbstractParasites can select for sexual reproduction in host populations, preventing replacement by faster growing asexual lineages. This is usually attributed to so-called “Red Queen Dynamics” (RQD), where antagonistic coevolution causes fluctuating selection in allele frequencies, which provides sex with an advantage over asex. However, parasitism may also maintain sex in the absence of RQD when sexual populations are more genetically diverse – and hence more resistant, on average – than clonal populations, allowing sex and asex to stably coexist. While the maintenance of sex due to RQD has been studied extensively, the conditions that allow sex and asex to stably coexist have yet to be explored in detail. In particular, we lack an understanding of how host demography and parasite epidemiology affect the maintenance of sex in the absence of RQD. Here, I use an eco-evolutionary model to show that both population density and the type and strength of virulence are important for maintaining sex, which can be understood in terms of their effects on disease prevalence and severity. In addition, I show that even in the absence of heterozygote advantage, asexual heterozygosity affects coexistence with sex due to variation in niche overlap. These results reveal which host and parasite characteristics are most important for the maintenance of sex in the absence of RQD, and provide empirically testable predictions for how demography and epidemiology mediate competition between sex and asex.


2017 ◽  
Vol 122 (4) ◽  
pp. 681-696 ◽  
Author(s):  
Matthias Hartmann ◽  
Michal Štefánek ◽  
Pavel Zdvořák ◽  
Petr Heřman ◽  
Jindřich Chrtek ◽  
...  

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