Repeated formation of correlated species in Tranzschelia (Pucciniales)

Heteroecism, or alternation between two unrelated hosts, is a widespread phenomenon among rust fungi (Pucciniales). In addition to heteroecism, rust fungi have evolved elaborate life cycles ranging from the five spore stages of macrocyclic species with many variations down to microcyclic species that may produce just two of these stages to complete their life cycles on a single host species. Considering the large number of nearly 8000 described rust fungi species and the high proportion that are host-alternating, heteroecism apparently is a successful strategy for these fungi, at least in terms of species diversity. However, the cost of maintaining a heteroecious strategy with respect to spore production and two different host plant species must be high. In Pucciniales, sister-species pairs that include one host-alternating (heteroecious) and one non-host-alternating (autoecious) species that share a common host are called correlated species. In this study, we tested Tranzschelia species for the existence of correlated species using molecular phylogenetic data. We reveal the presence of three pairs of correlated species within this single genus and suggest that this is a repeating process in the evolution of rust fungi. We show that a heteroecious macrocyclic strategy can be the starting point for deriving microcyclic autoecious species. The high cost of host alternation may be compensated by the fact that it is a facultative process in Tranzschelia with numerous strategies for the species to persist in one or the other host or as overwintering spore. Consequently, the advantage of host alternation seems higher than the cost of (facultative) heteroecism.