Rapid genetic change underpins antagonistic coevolution in a natural host‐pathogen metapopulation

Thrall, Peter H.; Laine, Anna‐Liisa; Ravensdale, Michael; Nemri, Adnane; Dodds, Peter N.; Barrett, Luke G.; Burdon, Jeremy J.

doi:10.1111/j.1461-0248.2012.01749.x

Cited by 203 publications

(223 citation statements)

References 59 publications

(141 reference statements)

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“…Coevolutionary dynamics between hosts and parasites is increasingly investigated using experimental evolution (15) and more specifically time-shift assays (16)(17)(18), in which hosts or parasites from a given time point are compared with their counterparts from the past or future, enabling the examination of putative reciprocal adaptations (19,20). Some of the prime experimental models are bacteria and their lytic phages, which exhibit rapid evolution and are amenable to time-shift tests.…”

mentioning

confidence: 99%

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Betts

Kaltz

Hochberg

2014

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

101

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Significance Scientists have long debated the dynamic form of perpetual reciprocal adaptations, or coevolution, between hosts and their parasites. The two main types of antagonistic coevolution described to date are arms race dynamics, in which interaction traits escalate through time, and fluctuating selection dynamics, in which traits cycle through time. We used experimental evolution between Pseudomonas aeruginosa and a panel of its lytic phages and found the full known range of coevolutionary dynamics. We argue that the coevolutionary pattern is determined by whether phages typically adsorb directly to receptors on the bacterial outer membrane or instead use retractable type IV pili as a primary or alternative site. Our results have applications in the use of phages as therapeutics or disinfectants to control bacterial pathogens.

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mentioning

confidence: 99%

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Betts

Kaltz

Hochberg

2014

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

101

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“…Thus, we speculate that barrier defences early in the infection process may play a crucial role in shaping the distribution of genetic variation for resistance in a given system. Barrier defences are also at the heart of gene-for-gene models in plant-pathogen interactions, which have been suggested to have an important role in Red Queenlike coevolutionary dynamics (Frank, 1993;Thrall et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Genetic architecture of resistance in Daphnia hosts against two species of host-specific parasites

Routtu

Ebert

2014

Heredity

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Understanding the genetic architecture of host resistance is key for understanding the evolution of host-parasite interactions. Evolutionary models often assume simple genetics based on few loci and strong epistasis. It is unknown, however, whether these assumptions apply to natural populations. Using a quantitative trait loci (QTL) approach, we explore the genetic architecture of resistance in the crustacean Daphnia magna to two of its natural parasites: the horizontally transmitted bacterium Pasteuria ramosa and the horizontally and vertically transmitted microsporidium Hamiltosporidium tvaerminnensis. These two systems have become models for studies on the evolution of host-parasite interactions. In the QTL panel used here, Daphnia's resistance to P. ramosa is controlled by a single major QTL (which explains 50% of the observed variation). Resistance to H. tvaerminnensis horizontal infections shows a signature of a quantitative trait based in multiple loci with weak epistatic interactions (together explaining 38% variation). Resistance to H. tvaerminnensis vertical infections, however, shows only one QTL (explaining 13.5% variance) that colocalizes with one of the QTLs for horizontal infections. QTLs for resistance to Pasteuria and Hamiltosporidium do not colocalize. We conclude that the genetics of resistance in D. magna are drastically different for these two parasites. Furthermore, we infer that based on these and earlier results, the mechanisms of coevolution differ strongly for the two host-parasite systems. Only the Pasteuria-Daphnia system is expected to follow the negative frequency-dependent selection (Red Queen) model. How coevolution works in the Hamiltosporidium-Daphnia system remains unclear.

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“…B 281: 20132567 predicted to covary positively with resistance, and negatively with tolerance as the cost of resistance decreases; or (ii) virulence is predicted to covary negatively with resistance, and positively with tolerance as the cost of tolerance decreases. According to experimental studies focusing on pathogen virulence, considerable spatial variation is observed in this three-component interaction, as well as in the strength of local coevolutionary dynamics [59]. Hence, demonstrating significant transmission across generations for tolerance and resistance is an important prerequisite for understanding coevolution between virulence, resistance and tolerance.…”

Section: Evolutionary Implications and Conclusionmentioning

confidence: 99%

Heritable variation in host tolerance and resistance inferred from a wild host–parasite system

et al. 2014

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Hosts have evolved two distinct defence strategies against parasites: resistance (which prevents infection or limit parasite growth) and tolerance (which alleviates the fitness consequences of infection). However, heritable variation in resistance and tolerance and the genetic correlation between these two traits have rarely been characterized in wild host populations. Here, we estimate these parameters for both traits in Leuciscus burdigalensis, a freshwater fish parasitized by Tracheliastes polycolpus. We used a genetic database to construct a full-sib pedigree in a wild L. burdigalensis population. We then used univariate animal models to estimate inclusive heritability (i.e. all forms of genetic and non-genetic inheritance) in resistance and tolerance. Finally, we assessed the genetic correlation between these two traits using a bivariate animal model. We found significant heritability for resistance (H ¼ 17.6%; 95% CI: 7.2-32.2%) and tolerance (H ¼ 18.8%; 95% CI: 4.4-36.1%), whereas we found no evidence for the existence of a genetic correlation between these traits. Furthermore, we confirm that resistance and tolerance are strongly affected by environmental effects. Our results demonstrate that (i) heritable variation exists for parasite resistance and tolerance in wild host populations, and (ii) these traits can evolve independently in populations.

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Rapid genetic change underpins antagonistic coevolution in a natural host‐pathogen metapopulation

Cited by 203 publications

References 59 publications

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Genetic architecture of resistance in Daphnia hosts against two species of host-specific parasites

Heritable variation in host tolerance and resistance inferred from a wild host–parasite system

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