Diversity and the maintenance of sex by parasites

Ashby, Ben; King, Kayla C.

doi:10.1111/jeb.12590

Cited by 22 publications

(47 citation statements)

References 61 publications

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“…Ecological feedbacks are crucial in shaping selection in both hosts and parasites (36)(37)(38)(39)(40)(41). Host defenses often reduce disease incidence at the population level, which decreases selection for defense mechanisms and increases selection for counter adaptations in the parasite.…”

Section: Discussionmentioning

confidence: 99%

Coevolution of parasite virulence and host mating strategies

Ashby

Boots

2015

Proc. Natl. Acad. Sci. U.S.A.

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Parasites are thought to play an important role in sexual selection and the evolution of mating strategies, which in turn are likely to be critical to the transmission and therefore the evolution of parasites. Despite this clear interdependence we have little understanding of parasite-mediated sexual selection in the context of reciprocal parasite evolution. Here we develop a general coevolutionary model between host mate preference and the virulence of a sexually transmitted parasite. We show when the characteristics of both the host and parasite lead to coevolutionarily stable strategies or runaway selection, and when coevolutionary cycling between high and low levels of host mate choosiness and virulence is possible. A prominent argument against parasites being involved in sexual selection is that they should evolve to become less virulent when transmission depends on host mating success. The present study, however, demonstrates that coevolution can maintain stable host mate choosiness and parasite virulence or indeed coevolutionary cycling of both traits. We predict that choosiness should vary inversely with parasite virulence and that both relatively long and short life spans select against choosy behavior in the host. The model also reveals that hosts can evolve different behavioral responses from the same initial conditions, which highlights difficulties in using comparative analysis to detect parasitemediated sexual selection. Taken as a whole, our results emphasize the importance of viewing parasite-mediated sexual selection in the context of coevolution.host-parasite coevolution | mate choice | virulence | transmission avoidance | sexually transmitted infection S ince Hamilton and Zuk (1) first proposed that parasitism may explain the existence of secondary sex traits such as the peacock's tail, there has been considerable interest in the role that parasites play in sexual selection and the evolution of mating strategies (2-19). A prominent theory, known as the transmissionavoidance hypothesis, posits that secondary sex traits, and more generally, mating strategies, have evolved to limit the risk of contracting an infection (10). Although this theory emphasizes the importance of parasites in determining mating strategies, it is clear that different mating strategies will have an impact on infectious disease transmission and therefore influence parasite evolution. However, despite this clear interdependence we lack a coevolutionary theory of mating strategies that captures reciprocal adaptations by both species.Sex can leave individuals at risk of infection due to sustained close contact with sexual partners or through the transfer of genetic material (20). Hence, sexually transmitted infections, which are common in both plants (21) and animals (22), are likely to be a key factor in the evolution of mating strategies. Furthermore, sexually transmitted infections typically exhibit different epidemiological dynamics (17, 23) and disease outcomes (e.g., sterility rather than mortality; ref. 22) to other in...

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Section: Discussionmentioning

confidence: 99%

Coevolution of parasite virulence and host mating strategies

Ashby

Boots

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Consistent with the idea that it is harder for a parasite to adapt to a heterogeneous host population 23 , virus rapidly evolved high levels of infectivity on monocultures, but not on a diverse mix of the same host genotypes. Parasites are often invoked as the selective force driving the evolution of diversity generating mechanisms 23–26 . In most cases, individual-level selection is assumed to be the driver of these traits, because individual benefits are high, and group selective benefits would be opposed by the invasion of individuals who do not pay the fitness costs associated with these mechanisms (for example, sex and increased mutation rates) 26–28 .…”

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confidence: 99%

“…Parasites are often invoked as the selective force driving the evolution of diversity generating mechanisms 23–26 . In most cases, individual-level selection is assumed to be the driver of these traits, because individual benefits are high, and group selective benefits would be opposed by the invasion of individuals who do not pay the fitness costs associated with these mechanisms (for example, sex and increased mutation rates) 26–28 . In the case of CRISPR-Cas, we speculate that population-level selection may have contributed to its evolution.…”

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confidence: 99%

The diversity-generating benefits of a prokaryotic adaptive immune system

Houte

Ekroth

Broniewski

et al. 2016

Nature

252

301

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Prokaryotic CRISPR-Cas adaptive immune systems insert spacers derived from viruses and other parasitic DNA elements into CRISPR loci to provide sequence-specific immunity1,2. This frequently results in high within-population spacer diversity3–6, but it is unclear if and why this is important. Here we show that, as a result of this spacer diversity, viruses can no longer evolve to overcome CRISPR-Cas by point mutation, which results in rapid virus extinction. This effect arises from synergy between spacer diversity and the high specificity of infection, which greatly increases overall population resistance. We propose that the resulting short-lived nature of CRISPR-dependent bacteria–virus coevolution has provided strong selection for the evolution of sophisticated virus-encoded anti-CRISPR mechanisms7.

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“…The RQH predicts that sexually reproducing hosts overcome the cost of sex under strong parasitic pressure by producing genetically diverse offspring that can escape infection (Haldane, 1949;Jaenike, 1978;Hamilton, 1980;Hamilton et al, 1990). Limited genetic diversity of asexually reproducing hosts allows for sexual reproduction to be maintained in the host population (Ashby and King, 2015).…”

Section: Introductionmentioning

confidence: 99%

Bridging the gap between theory and data: the Red Queen Hypothesis for sex

Park

Bolker

2019

Preprint

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Sexual 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.

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Diversity and the maintenance of sex by parasites

Cited by 22 publications

References 61 publications

Coevolution of parasite virulence and host mating strategies

Coevolution of parasite virulence and host mating strategies

The diversity-generating benefits of a prokaryotic adaptive immune system

Bridging the gap between theory and data: the Red Queen Hypothesis for sex

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