Greater Phage Genotypic Diversity Constrains Arms-Race Coevolution.

Meaghan Castledine,Pawel Sierocinski,Alex Hayward,Mhairi Inglis,Suzanne Kay,Daniel Padfield,Angus Buckling

doi:10.3389/fcimb.2022.834406

Meaghan Castledine, Pawel Sierocinski + Show 5 more

Open Access

https://doi.org/10.3389/fcimb.2022.834406

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Abstract

Antagonistic coevolution between hosts and parasites, the reciprocal evolution of host resistance and parasite infectivity, has important implications in ecology and evolution. The dynamics of coevolution—notably whether host or parasite has an evolutionary advantage—is greatly affected by the relative amount of genetic variation in host resistance and parasite infectivity traits. While studies have manipulated genetic diversity during coevolution, such as by increasing mutation rates, it is unclear how starting genetic diversity affects host–parasite coevolution. Here, we (co)evolved the bacterium Pseudomonas fluorescens SBW25 and two bacteriophage genotypes of its lytic phage SBW25ɸ2 in isolation (one phage genotype) and together (two phage genotypes). Bacterial populations rapidly evolved phage resistance, and phage reciprocally increased their infectivity in response. When phage populations were evolved with bacteria in isolation, bacterial resistance and phage infectivity increased through time, indicative of arms-race coevolution. In contrast, when both phage genotypes were together, bacteria did not increase their resistance in response to increasing phage infectivity. This was likely due to bacteria being unable to evolve resistance to both phage via the same mutations. These results suggest that increasing initial parasite genotypic diversity can give parasites an evolutionary advantage that arrests long-term coevolution. This study has important implications for the applied use of phage in phage therapy and in understanding host–parasite dynamics in broader ecological and evolutionary theory.

Highlights

Antagonistic coevolution between hosts and parasites, the reciprocal evolution of host resistance and parasite infectivity, has important implications for a range of ecological and evolutionary processes (Brockhurst and Koskella, 2013; Jephcott et al, 2016)
The ancestral-type phage (P1) differed by few, only three SNPs to the reference SBW25ɸ2, with one of these SNPs being in the tail-fibre gene which is known to be important for phage infectivity (Scanlan et al, 2011)
The dynamics of bacteria resistance and phage infectivity evolution differed between monoculture and when both phage genotypes were present, even though the genotypes only differed by 8 genetic variants (SNPs and indels)

Summary

Introduction

Antagonistic coevolution between hosts and parasites, the reciprocal evolution of host resistance and parasite infectivity, has important implications for a range of ecological and evolutionary processes (Brockhurst and Koskella, 2013; Jephcott et al, 2016). Of key importance is which species has the evolutionary advantage in the interaction and, is better adapted (Brockhurst and Koskella, 2013). Genotypic Diversity Constrains Arms-Race Coevolution variation underpinning host defense and parasite infectivity traits (Dybdahl et al, 2014). Most studies to date have investigated conditions where differences in genetic variation between host and parasite are manipulated throughout coevolution (Morgan et al, 2005; Morran et al, 2011; Brockhurst and Koskella, 2013; Savolainen et al, 2013; Jephcott et al, 2016; Zhang and Buckling, 2016). Is any advantage to host or parasite short lived or does initial diversity have implications for long-term coevolutionary dynamics?

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