Host-pathogen coevolution increases genetic variation in susceptibility to infection.

Elizabeth Ml Duxbury,Sophia Cl Smith,Robert L Unckless,Lucia Tagliaferri,Ben Longdon,Luca Love,Jonathan P Day,Yannik Thüringer,Imogen Lindsley,Ignacio Tolosana,Davide Maria Vespasiani,Altug Kamacioglu,Francis M Jiggins

doi:10.7554/elife.46440

Abstract

It is common to find considerable genetic variation in susceptibility to infection in natural populations. We have investigated whether natural selection increases this variation by testing whether host populations show more genetic variation in susceptibility to pathogens that they naturally encounter than novel pathogens. In a large cross-infection experiment involving four species of Drosophila and four host-specific viruses, we always found greater genetic variation in susceptibility to viruses that had coevolved with their host. We went on to examine the genetic architecture of resistance in one host species, finding that there are more major-effect genetic variants in coevolved host-pathogen interactions. We conclude that selection by pathogens has increased genetic variation in host susceptibility, and much of this effect is caused by the occurrence of major-effect resistance polymorphisms within populations.

Highlights

From bacteria to plants and insects to humans, it is common to find considerable genetic variation in susceptibility to infection in natural populations (Chapman and Hill, 2012; Bangham et al, 2008a; Hammond-Kosack and Jones, 1997; Lazzaro et al, 2004)
We have found greater genetic variation in susceptibility to viruses that naturally infect Drosophila compared to viruses that do not, suggesting that selection by these pathogens has acted to increase the amount of genetic variation in susceptibility
This effect was largely caused by a modest number of major-effect genes that explain over half of the genetic variance in resistance

Summary

Introduction

From bacteria to plants and insects to humans, it is common to find considerable genetic variation in susceptibility to infection in natural populations (Chapman and Hill, 2012; Bangham et al, 2008a; Hammond-Kosack and Jones, 1997; Lazzaro et al, 2004). This variation in susceptibility can determine the impact of disease on health and economic output (Cooke and Hill, 2001; King and Lively, 2012; Alonso-Blanco and Mendez-Vigo, 2014; Burgner et al, 2006). Understanding the origins of genetic variation in susceptibility is a fundamental question in infectious disease biology

Objectives

Methods

Results

Conclusion