Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini

Abstract

Many pathogens undergo both sexual and asexual reproduction to varying degrees, yet the ecological, genetic and evolutionary consequences of different reproductive strategies remain poorly understood. Here we investigate the population genetic structure of wild populations of the plant pathogen Melampsora lini on its host Linum marginale, using amplified fragment length polymorphism (AFLP) markers, two genes underlying pathogen virulence, and phenotypic variation in virulence. In Australia, M. lini occurs as two genetically and geographically divergent lineages (AA and AB), one of which is completely asexual (AB), and the other able to reproduce both clonally and sexually (AA). To quantify the genetic and evolutionary consequences of these different life histories, we sampled five populations in each of two biogeographical regions. Analysis of AFLP data obtained for 275 isolates revealed largely disjunct geographical distributions for the two different lineages, low genetic diversity within lineages, and strong genetic structure among populations within each region. We also detected significant divergence among populations for both Avr genes and virulence phenotypes, although generally these values were lower than those obtained with AFLP markers. Furthermore, isolates belonging to lineage AA collectively harboured significantly higher genotypic and phenotypic diversity than lineage AB isolates. Together these results illustrate the important roles of reproductive modes and geographical structure in the generation and maintenance of virulence diversity in populations of M. lini.

Fig. 1

Map with insert region showing locations of study regions and populations in New South Wales, Australia.

Fig. 2

UPGMA phylogram based on pairwise estimates of Nei’s genetic distance (AFLP) among populations of Melampsora lini.

Fig. 3

Principal coordinates plots based on Euclidean distances among multilocus AFLP genotypes for all clone corrected isolates from plains and mountains populations. (a) Lineage AA isolates (n = 100), axes explain 56.6% (36.5 + 20.1) of the variation. (b) Lineage AB isolates (n = 83), axes explain 73.2% (56.1 + 17.1) of the variation.

Fig. 4

Histograms of frequencies of different AFLP multilocus genotypes including more than one individual out of a total of 275 isolates of Melampsora lini. Lineage AA and AB isolates had no multilocus genotypes in common. (a) Lineage AA isolates. A total of 83 multilocus genotypes were recovered from 124 isolates, with 11 occurring more than once. (b) Lineage AB isolates. A total of 25 multilocus genotypes were recovered from 151 isolates, with 10 occurring more than once.

Fig. 5

Virulence profile of lineage AA and AB isolates. (a) Histograms of frequencies of different virulence phenotypes (including more than one individual) among 124 lineage AA and 151 lineage AB isolates of Melampsora lini as determined on 11 differential host lines collected from plains and mountains populations. Individual virulence phenotypes represent a unique combination of virulence specificities on the differential set, and have been assigned an arbitrary number as shown on the x-axis. (b) Mean virulence responses of isolates of M. lini belonging to lineage AA and AB on differential lines of the host plant Linum marginale.