Host–parasite coevolution induces selection for condition‐dependent sex

Abstract

Sex and recombination remain one of the biggest riddles of evolutionary biology. One of the most prominent hypotheses, the Red Queen Hypothesis, claims that sex has evolved as a means to efficiently create genotypes that are resistant against coevolving parasites. However, previous models of the Red Queen have assumed that all individuals are equally likely to engage in sexual reproduction, regardless of their infection status, an assumption that may not be true in reality. Here, we consider a population genetic model of a host population coevolving with a parasite population, where the parasites are haploid and the hosts either haploid or diploid. We assume that the probability to engage in sex may be different in infected and uninfected hosts and ascertain the success of different reproductive strategies with a modifier-gene approach. Our model shows that in the large majority of the parameter space, infection-dependent sex is more successful than infectionindependent sex. We identify at least two reasons for this: (i) an immediate short-term advantage of breaking-down gene combinations of unfit individuals and (ii) a selfish spread of the condition-dependent modifiers, in analogy to the 'abandon-ship' effect in single species. In diploids, these effects are often powerful enough to overcome the detrimental effects of segregation. These results raise the intriguing question of why infection-induced sex is not more commonly observed in nature.

Genetic conflict, kin and the origins of novel genetic systems

“…This may help to explain one aspect of the distribution of genetic systems: the near-absence of obligate parthenogenesis from marine environments, in comparison to reasonably high frequency in some terrestrial and freshwater environments (table 1). This observation may be understandable in terms of the Parasite Red Queen hypothesis for the adaptive significance of sex [71,72]. When we left the ocean, we may have left most of our pathogens and parasites behind and thus are less reliant on sex than marine organisms are.…”

Condition-dependent sex: who does it, when and why?

“…According to the Red Queen hypothesis [54,55], coevolution of hosts and pathogens produces oscillations in the frequencies of different genotypes and can favour the evolution of sex. In such cases, theoretical models suggest that infection-dependent sex is even more successful than infection-independent sex [17].…”

“…In essence, an allele that regulates a facultative reproductive system could benefit from following the abandon-ship principle [9]: switching to sexual reproduction in maladapted individuals but reproducing asexually in well-adapted ones, thereby associating itself with good genetic backgrounds (figure 2). This advantage can drive the evolution of condition-dependent sex under different scenarios, including mutation-selection balance [9], adaptation [13] and host parasite coevolution [17].…”

Allocation, not male resistance, increases male frequency during epidemics: a case study in facultatively sexual hosts

“…An alternative, “Abandon Ship” hypothesis links stress to sex (Hadany and Otto , Mostowy and Engelstädter ). Stressors including drought, starvation, crowding, and predators can drive increased allocation to sex in a diverse array of organisms including facultative parthenogens (e.g., Daphnia [Cáceres and Tessier 2004], moths [Kumpulainen et al.…”