Local maladaptation of the anther-smut fungus parasitizing Dianthus carthusianorum

Abstract

Pathogens are generally expected to evolve faster than their hosts and are therefore likely to be locally adapted. However, some pathogens might lag behind in the co-evolutionary arms race because they do not have some of the advantages shared by most other pathogens (e.g., high mutation or recombination rates, short generation time, high dispersal ability). This is the case of Microbotryum fungi that cause the anther smut disease in plants of the family Caryophyllaceae. We investigated the patterns of local adaptation and maladaptation in Microbotryum carthusianorum and its host plant Dianthus carthusianorum. We performed a full cross-inoculation experiment using half-sib plant families and fungal samples originating from three naturally infected populations in the Czech Republic. We specifically asked, which components of pathogen fitness (i.e., infectivity and host manipulation) are affected by local (mal)adaptation. The pathogen was on average 1.6 times more successful in infecting plants from foreign populations compared to plants from its home population. Once the infection was successful, the pathogen accelerated the plant’s flowering and thus increased the opportunity for transmission to new hosts. However, the level of manipulation of host flowering did not differ between home and foreign populations. This study showed that the pathogen’s infectivity followed a clear pattern of local maladaptation, whereas the host manipulation did not. Our study taken together with previous studies of a related anther smut species reveals the pervasiveness of local maladaptation in this group of pathogens that arises as the result of their restricted gene flow and reduced recombination rates.