Inferring phylogeny and speciation of Gymnosporangium species, and their coevolution with host plants

Abstract

Gymnosporangium species (Pucciniaceae, Pucciniales) cause serious diseases and significant economic losses to apple cultivars. Most of the reported species are heteroecious and complete their life cycles on two different plant hosts belonging to two unrelated genera, i.e. Juniperus and Malus. However, the phylogenetic relationships among Gymnosporangium species and the evolutionary history of Gymnosporangium on its aecial and telial hosts were still undetermined. In this study, we recognized species based on rDNA sequence data by using coalescent method of generalized mixed Yule-coalescent (GMYC) and Poisson Tree Processes (PTP) models. The evolutionary relationships of Gymnosporangium species and their hosts were investigated by comparing the cophylogenetic analyses of Gymnosporangium species with Malus species and Juniperus species, respectively. The concordant results of GMYC and PTP analyses recognized 14 species including 12 known species and two undescribed species. In addition, host alternations of 10 Gymnosporangium species were uncovered by linking the derived sequences between their aecial and telial stages. This study revealed the evolutionary process of Gymnosporangium species, and clarified that the aecial hosts played more important roles than telial hosts in the speciation of Gymnosporangium species. Host switch, losses, duplication and failure to divergence all contributed to the speciation of Gymnosporangium species.

Figure 1. Phylogenetic trees of the combined data of the internal transcribed spacer regions and intervening 5.8S nrRNA gene (ITS) and the large subunit (LSU) rDNA obtained from parsimony analysis.

Bayesian posterior probabilities (Bpp) were given immediately followed by the bootstrap values of ML on the nodes in the topology. Asterisk (*) represented bootstrap values less than 50% or Bpp less than 0.75 in the topology. The first column depicts species recognized by the single-threshold GMYC model, and second column depicts putative species recognized by multiple-threshold GMYC model. The third column depicts putative species recognized by PTP model. The name of each putative species was designated based mainly on Kern (1973).

Figure 2. Divergence time estimation of Gymnosporangium species using the rDNA dataset.

The chronogram was obtained from the molecular clock analysis using BEAST. The Ravenelia (Raveneliaceae, Pucciniales) fossil was served as a reliable calibration point to estimate the divergent time of Gymnosporangium species. Species with aecial host on Malus species were indicated in red color. The estimated divergence time of telial and aecial hosts were indicated below the geographic time scale. In addition, the potential number of telial and aecial host genera was pointed out following the name of the species based on Kern (1973) and our study.

Figure 3. The tanglegram between specimens of Gymnosporangium species and telial host Juniperus rDNA phylogenies.

Fungal (right) and host (left) phylogenies from Bayesian inference were used to generate the tanglegram using TreeMap 3.0ß.

Figure 4. The tanglegram between specimens of Gymnosporangium species and aecial host Malus rDNA phylogenies.

Fungal (right) and host (left) phylogenies from Bayesian inference were used to generate the tanglegram using TreeMap 3.0ß.

Figure 5. Cophylogenetic analysis of the Gymnosporangium–Juniperus pathosystem conducted with Jane 4 and using phylogenies including one representative per potential species of parasite and host.

Black branches represent the host phylogeny and blue branches the parasite phylogeny. Violet lines represent original polytomies resolved by Jane to minimize the overall cost of the solution. The cost regime used for the reconstruction was by following event costs: (cospeciation = 2, duplication = 0, host switch = 1, lineage sorting = 1 and failure to diverge = 1). The best-fit reconciliation of the Gymnosporangium and Juniperus trees included 6 duplications, four host switches, three losses and finally four failures to diverge.

Figure 6. Cophylogenetic analysis of the Gymnosporangium–Malus pathosystem conducted with Jane 4 and using phylogenies including one representative per potential species of parasite and host.

Black branches represent the host phylogeny and blue branches the parasite phylogeny. The cost regime used for the reconstruction was by following event costs: (cospeciation = 2, duplication = 0, host switch = 0, lineage sorting = 1 and failure to diverge = 0). The best-fit reconciliation of the Gymnosporangium and Malus trees included four duplications, seven host switches, fifteen losses and four failures to divergence.