Strong phylogeographic co‐structure between the anther‐smut fungus and its white campion host

Abstract

Although congruence between host and pathogen phylogenies has been extensively investigated, the congruence between host and pathogen genetic structures at the within-species level has received little attention. Using an unprecedented and comprehensive collection of associated plant-pathogen samples, we investigated the degree of congruence between the genetic structures across Europe of two evolutionary and ecological model organisms, the anther-smut pathogen Microbotryum lychnidis-dioicae and its host plant Silene latifolia. We demonstrated a significant and particularly strong level of host-pathogen co-structure, with three main genetic clusters displaying highly similar spatial ranges in Western Europe, Eastern Europe and Italy, respectively. Correcting for the geographical component of genetic variation, significant correlations were still found between the genetic distances of anther-smut and host populations. Inoculation experiments suggested plant local adaptation, at the cluster level, for resistance to pathogens. These findings indicate that the pathogen remained isolated in the same fragmented southern refugia as its host plant during the last glaciation, and that little long-distance dispersal has occurred since the recolonization of Europe for either the plant or the pathogen, despite their known ability to travel across continents. This, together with the inoculation results, suggests that coevolutionary and competitive processes may be drivers of host-pathogen co-structure.

Multiple infections, relatedness and virulence in the anther‐smut fungus castrating Saponaria plants

“…The anther‐smut parasitizing the two Saponaria species showed genetic subdivision with several distinct genetic clusters. These clusters, however, showed no geographical pattern consistent with glacial refugia such as was found previously for M. lychnidis‐dioicae across Europe (Feurtey et al., ; Gladieux et al., ; Vercken et al., ). Each cluster spanned most of the geographical range of sampling, indicating that interactions and competition may frequently occur between individuals belonging to different clusters.…”

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

“…Studies of population genetic structure and divergence in plant fungal pathogens have so far mostly focused on crop pathogens (Barrès et al, 2008; Enjalbert, Duan, Leconte, HovmøLler, & De Vallavieille‐Pope, 2005; Fournier & Giraud, 2008; Linde, Zhan, & McDonald, 2002; Saleh, Milazzo, Adreit, Fournier, & Tharreau, 2014; Stukenbrock, Banke, & McDonald, 2006; Zaffarano, McDonald, & Linde, 2008), in which patterns are heavily impacted by host genetic homogeneity and high abundance, as well as by human‐mediated plant and pathogen dispersal. Here we found strong congruence in population structure between hosts and pathogens, in agreement with a previous study on other anther‐smut lineages (Feurtey et al, 2016). Further studies on other natural systems are needed to assess whether this represents a general pattern in natural pathogen–host communities.…”

“…The significant IBD pattern in both the S. nutans plant and anther‐smut fungi and the correlation between the genetic distances between host and pathogen pairs when controlling for IBD suggest that the anther‐smut fungi followed similar recolonization routes as the plant and/or became specialized on the host genetic lineages. However, contrary to the S. latifolia – Microbotryum lychnidis‐dioicae system (Feurtey et al, 2016) and other host–pathogen systems (Barrett et al, 2008; Criscione, Poulin, & Blouin, 2005; Nieberding et al, 2008; Nieberding & Olivieri, 2007), we found higher levels of subdivision in S. nutans than in its associated anther‐smut fungi. The weaker genetic structure in anther smut fungi compared to its host again suggests extinction of the pathogen lineage in a plant lineage, followed by recolonization from another fungal lineage, or the ability of an anther‐smut lineage to remain generalist on two closely related plant lineages.…”

Co‐occurrence among three divergent plant‐castrating fungi in the same Silene host species

“…Differentiation in disjunct refugia during the last glaciation in Europe may also have shaped differential adaptation to abiotic conditions and/or generated allopatry. Strong population differentiation has been found in other Microbotryum species that reflects footprints of persistence in glaciation refugia, for example, in M. lychnidis‐dioicae parasitizing S. latifolia (Badouin et al., ; Feurtey et al., ; Gladieux et al., ; Vercken et al., ) and M. silenes‐acaulis parasitizing S. acaulis (Bueker et al., ). High selfing rates were inferred for previously studied Microbotryum species (Bueker et al., ; Giraud, ; Gladieux et al., ; Hood & Antonovics, , ), and such a closed mating system may contribute to generate and maintain strong population structure and genetic isolation between species (Gibson, Hood, & Giraud, ; Vercken et al., ).…”