Neutral genomic signatures of host-parasite coevolution

Daniel Živković,Sona John,Mélissa Verin,Aurélien Tellier,Wolfgang Stephan

doi:10.1186/s12862-019-1556-3

Daniel Živković, Sona John + Show 3 more

Open Access

https://doi.org/10.1186/s12862-019-1556-3

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Abstract

BackgroundCoevolution is a selective process of reciprocal adaptation in hosts and parasites or in mutualistic symbionts. Classic population genetics theory predicts the signatures of selection at the interacting loci of both species, but not the neutral genome-wide polymorphism patterns. To bridge this gap, we build an eco-evolutionary model, where neutral genomic changes over time are driven by a single selected locus in hosts and parasites via a simple biallelic gene-for-gene or matching-allele interaction. This coevolutionary process may lead to cyclic changes in the sizes of the interacting populations.ResultsWe investigate if and when these changes can be observed in the site frequency spectrum of neutral polymorphisms from host and parasite full genome data. We show that changes of the host population size are too smooth to be observable in its polymorphism pattern over the course of time. Conversely, the parasite population may undergo a series of strong bottlenecks occurring on a slower relative time scale, which may lead to observable changes in a time series sample. We also extend our results to cases with 1) several parasites per host accelerating relative time, and 2) multiple parasite generations per host generation slowing down rescaled time.ConclusionsOur results show that time series sampling of host and parasite populations with full genome data are crucial to understand if and how coevolution occurs. This model provides therefore a framework to interpret and draw inference from genome-wide polymorphism data of interacting species.

Highlights

Host-parasite antagonistic interactions are a role model for observing and studying rapid evolutionary change as well as feedbacks between ecological and evolutionary forces and time scales
The first key aspect of our eco-evolutionary framework is that changes in the population size are a direct consequence of the dynamics of the model (Eqs. (1) and (2), Additional file 1: SI1-SI3, driven by a single locus underpinning coevolution, and not assumed to follow an arbitrarily chosen function of time as in the majority of the population genetics literature
The reference population size Nref at the onset of an epidemics is important because 1) it sets up the initial available diversity, and 2) it defines the time scale for genetic drift in host and parasite and the timing of new neutral mutations occurring with rate θ

Summary

Introduction

Host-parasite antagonistic interactions are a role model for observing and studying rapid evolutionary change as well as feedbacks between ecological and evolutionary forces and time scales. Coevolution, defined here as the reciprocal adaptation of hosts and their parasites, typically generates significant phenotypic and genetic diversity for host resistance and for parasite infectivity and virulence Such changes in the genetic composition of the interacting species at the key underpinning loci, drive, and are driven by, short-term epidemiological (ecological) dynamics. Classic population genetics theory predicts the signatures of selection at the interacting loci of both species, but not the neutral genome-wide polymorphism patterns To bridge this gap, we build an eco-evolutionary model, where neutral genomic changes over time are driven by a single selected locus in hosts and parasites via a simple biallelic gene-for-gene or matching-allele interaction. This coevolutionary process may lead to cyclic changes in the sizes of the interacting populations

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