When does parasitism maintain sex in the absence of Red Queen Dynamics?

Ben Ashby

doi:10.1111/jeb.13718

Abstract

Parasites can select for sexual reproduction in host populations, preventing replacement by faster-growing asexual genotypes. 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 coexist at a stable equilibrium. Although 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.

Highlights

The question of why so many organisms reproduce sexually rather than asexually has been a long-standing puzzle in evolutionary biology (Maynard Smith, 1978)
This cycling in allele frequencies due to antagonistic coevolution is often referred to as Red Queen Dynamics (RQD) in the literature, this is a broader term which encompasses cycles that are not driven by negative frequency-dependent selection, and successive selective sweeps (Brockhurst et al, 2014)
(2010b) showed that it is possible for sexual and asexual hosts to coexist in the absence of RQD when the cost of producing males is offset by lower disease prevalence, on average

Summary

Introduction

The question of why so many organisms reproduce sexually rather than asexually has been a long-standing puzzle in evolutionary biology (Maynard Smith, 1978). Many studies assume that the advantages of sex are only realised when host and parasite populations exhibit negative frequency-dependent selection, as this can result in cyclical allele frequency dynamics and a continually varying environment with no fixed optimal phenotype. This cycling in allele frequencies due to antagonistic coevolution is often referred to as Red Queen Dynamics (RQD) in the literature, this is a broader term which encompasses cycles that are not driven by negative frequency-dependent selection, and successive selective sweeps (Brockhurst et al, 2014). While an asexual lineage may initially have a population growth rate advantage, this is eventually curtailed by higher levels of infection, which allows the two populations to coexist

Methods

Results

Conclusion