Abstract

How generalist parasites with wide host ranges can evolve is a central question in parasite evolution. Albugo candida is an obligate biotrophic parasite that consists of many physiological races that each specialize on distinct Brassicaceae host species. By analyzing genome sequence assemblies of five isolates, we show they represent three races that are genetically diverged by ∼1%. Despite this divergence, their genomes are mosaic-like, with ∼25% being introgressed from other races. Sequential infection experiments show that infection by adapted races enables subsequent infection of hosts by normally non-infecting races. This facilitates introgression and the exchange of effector repertoires, and may enable the evolution of novel races that can undergo clonal population expansion on new hosts. We discuss recent studies on hybridization in other eukaryotes such as yeast, Heliconius butterflies, Darwin's finches, sunflowers and cichlid fishes, and the implications of introgression for pathogen evolution in an agro-ecological environment.

Highlights

  • Most parasites have a restricted host range and are often unable to exploit even closely related hosts (Thompson, 2005; Poulin and Keeney, 2014)

  • The questions we addressed in the present study are: (1) Are the distinct physiological A. candida races genetically isolated and ‘on the road to speciation’? (2) Does suppression of host innate immunity enable cohabitation and growth of races with non-overlapping host ranges? To answer these questions, we generated genome sequence assemblies of five isolates that were collected from four host species (Brassica oleracea, Brassica juncea, Capsella bursa-pastoris, and Arabidopsis thaliana)

  • A. candida comprises distinct races that specialize on different plant species (Liu et al, 1996; Rimmer et al, 2000) and its physiological races can infect over 200 species of plants

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Summary

Introduction

Most parasites have a restricted host range and are often unable to exploit even closely related hosts (Thompson, 2005; Poulin and Keeney, 2014). Compared to necrotrophs that reproduce on dead plant material, obligate biotrophic parasites can only reproduce on living tissue, and are intimately associated with their hosts (Thines, 2014). This might be expected to result in host specialization. The adaptive evolution of, for example, new effectors that enable more efficient exploitation of one host species, increases the risk of detection in other host species by triggering their immune system (Martin and Kamoun, 2012) Due to this trade-off, the saying ‘Jack of all trades, master of none’ is especially true for obligate biotrophic parasites, because natural selection that maximises parasite fitness on one particular host species might lead to specialisation and reduced host range (e.g., Dong et al, 2014). There are generalist biotrophic parasites that appear to have overcome this evolutionary dilemma and show virulence on diverse hosts

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