Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: Prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation

Abstract

BackgroundUsing phylogenetic approaches, the expectation that parallel cladogenesis should occur between parasites and hosts has been validated in some studies, but most others provided evidence for frequent host shifts. Here we examine the evolutionary history of the association between Microbotryum fungi that cause anther smut disease and their Caryophyllaceous hosts. We investigated the congruence between host and parasite phylogenies, inferred cospeciation events and host shifts, and assessed whether geography or plant ecology could have facilitated the putative host shifts identified.For cophylogeny analyses on microorganisms, parasite strains isolated from different host species are generally considered to represent independent evolutionary lineages, often without checking whether some strains actually belong to the same generalist species. Such an approach may mistake intraspecific nodes for speciation events and thus bias the results of cophylogeny analyses if generalist species are found on closely related hosts. A second aim of this study was therefore to evaluate the impact of species delimitation on the inferences of cospeciation.ResultsWe inferred a multiple gene phylogeny of anther smut strains from 21 host plants from several geographic origins, complementing a previous study on the delimitation of fungal species and their host specificities. We also inferred a multi-gene phylogeny of their host plants, and the two phylogenies were compared. A significant level of cospeciation was found when each host species was considered to harbour a specific parasite strain, i.e. when generalist parasite species were not recognized as such. This approach overestimated the frequency of cocladogenesis because individual parasite species capable of infecting multiple host species (i.e. generalists) were found on closely related hosts. When generalist parasite species were appropriately delimited and only a single representative of each species was retained, cospeciation events were not more frequent than expected under a random distribution, and many host shifts were inferred.Current geographic distributions of host species seemed to be of little relevance for understanding the putative historical host shifts, because most fungal species had overlapping geographic ranges. We did detect some ecological similarities, including shared pollinators and habitat types, between host species that were diseased by closely related anther smut species. Overall, genetic similarity underlying the host-parasite interactions appeared to have the most important influence on specialization and host-shifts: generalist multi-host parasite species were found on closely related plant species, and related species in the Microbotryum phylogeny were associated with members of the same host clade.ConclusionWe showed here that Microbotryum species have evolved through frequent host shifts to moderately distant hosts, and we show further that accurate delimitation of parasite species is essential for interpreting cophylogeny studies.

Silene as a model system in ecology and evolution

“…Partial premating isolation among host plants also affects Microbotryum because the pathogen transmission depends on the host plants' habitats and pollinators (van Putten et al, 2007). There has however been little, if any, cospeciation between the plants and the fungi (Refrégier et al, 2008). Premating barriers between both close plant and fungal species are weak, making this system an ideal one to evaluate the importance of host and pathogen hybridization in disease evolution (Le Gac et al, 2007b;Karrenberg and Favre, 2008;Minder and Widmer, 2008;Sloan et al, 2008a).…”

A time and space complexity reduction for coevolutionary analysis of trees generated under both a Yule and Uniform model

“…This set includes evolutionary data from a number of fields including but not limited to, pathogens and their hosts (Charleston and Robertson, 2002), plant-insect relationships (McLeish et al, 2007), the evolutionary dependencies between plants and fungi (Refrégier et al, 2008), parasitic (Page et al, 2004) and mutualistic (Jackson, 2004) coevolution, and biogeography (Badets et al, 2011). The aim of this data set is to ensure that the running time improvements offered by the newly proposed data structure are consistent across the full spectrum of coevolutionary instances.…”

An improved node mapping algorithm for the cophylogeny reconstruction problem

“…Costs schemes vectors Reported map cost Data-set 1 (Hafner & Nadler 1988) Maximising codivergence −7 Jungles 8 Reconciliation 20 Data-set 2 (Paterson et al 2000) Maximising codivergence −10 Jungles 12 Reconciliation 27 Data-set 3 (Jackson 1999) Maximising codivergence −11 Jungles 13 Reconciliation 32 Data-set 4 (Refrégier et al 2008) Maximising codivergence −11 Jungles 34 Reconciliation 91 Data-set 5 (Sorenson et al 2004) Maximising codivergence −12 Jungles 29 Reconciliation 89 Data-set 6 (Percy et al 2004) Maximising codivergence −19 Jungles 62 Reconciliation 196 Figure 3. The running time of the original node mapping algorithm (Jane 1) and the new node mapping algorithm plotted on a logarithmic scale.…”