Figure 1.
The emergent trilobed flower of Hydnora visseri.
This photograph was taken at the type locality (Farm Namuskluft) in the Richtersveld region of southwestern Namibia. The host of H. visseri is Euphorbia gummifera at the type location (host not pictured).
Table 1.
Single copy nuclear genes used in the 19-gene-matrix.
Annotations are given for the indicated Arabidopsis gene.
Figure 2.
Phylogenetic origin of Hydnoraceae within photosynthetic Piperales.
To compare the performance of individual marker combinations, separate analyses were run and are summarized here. The plastid rbcL and atpB genes are not available for Hydnoraceae. The phylogenetic trees are displayed at the ordinal level, but zoomed in to family level within Piperales (blue). Hydnoraceae are highlighted in red. Both Maximum Likelihood and Bayesian Inference were applied. Nodes with less than 0.85 posterior probability (PP) were collapsed, while nodes with less than 50% bootstrap support (BS) are indicated with a dash. Support values are plotted above branches (PP first, BS second). The obtained topologies are congruent at these levels, but vary in resolution within Piperales. The concatenated dataset that contains all markers (Figure 2D) provides both the best resolution and best support values. In this tree, all Piperales families are statistically supported as monophyletic (considering PP values). Nuclear ribosomal and mitochondrial markers have been calculated separately as well, but those phylogenetic hypotheses are poorly resolved (Figure S1E–F).
Figure 3.
Relative substitution rates of nuclear single copy genes (nSCG) are elevated.
The relative substitution rates are shown for five partitioned datasets representing major Piperales lineages. In general, nSCG contribute significantly to the overall rate of the 19-gene-matrix in the different Piperales lineages. Within Hydnoraceae, rates of nSCG regions are 2–3 fold greater than nuclear ribosomal DNA (nrDNA) or mitochondrial DNA (mtDNA). However, comparing the relative rate of Hydnoraceae with other Piperales, the nSCG regions do not exceed the rate of other photosynthetic member such as Verhuellioideae. The partition of nSCG for Piperales is reduced from 14 to the 8 most complete genes for these lineages. Rates were compared using GRate (http://bioinfweb.info/Software/GRate) for different Piperales lineages using Canellales (Canella) as the reference and all other sampled taxa as outgroups.
Figure 4.
The holoparasitic Hydnoraceae originated in the Late Cretaceous.
A chronogram of the 19-gene-matrix applying a relaxed molecular clock using BEAST shows Hydnoraceae (red) originating in the Late Cretaceous (91 MYA) with a crown age of 55 MYA. The photosynthetic members of Piperales are highlighted in blue. The age, estimated with BEAST [66], is mapped on the right of the respective node in MYA and the highest posterior density (HPD) interval is indicated by a grey bar. The same calibration points and topological constraints have been applied to this dataset as well as to the Barkman et al. [10] dataset to ensure comparability (for the latter see Table 2, Figure S3, and for details the methods).
Table 2.
Relaxed molecular clock stem group age (SGA) and crown group age (CGA) estimates for angiosperm parasitic lineages, based on the four mitochondrial marker dataset [10].
Figure 5.
The “temporal specialization hypothesis” (TSH) postulates increasing specialization during the evolution of parasitism in plants.
Relationship of stem age, species number, host range, trophic type and host attachment site of the parasitic lineages is shown. The estimated age of each parasite lineage is plotted relative to lineage size (the species numbers are taken from the review by Westwood et al. [51]). The color of the symbol represents the trophic type for the indicated lineage (blue: autotrophic; yellow: hemiparasitic; red: holoparasitic), the shape indicates the mode of attachment (square: root parasite; round: stem parasite; rhomb: stem and root parasite; rimmed: endophytic) and the size represents host range (large: generalist on more than five families; medium: intermediate host range of two to five families; small: specialist on only one host family; shaded: all types of host ranges). Santalales and Balanophoraceae are plotted separately and together since phylogenetic analyses to date are inconclusive about the origin of Balanophoraceae within Santalales [36]. As the host range is difficult to capture, we chose three categories. A lineage is categorized by the typical host range and exceptions may exist. For Hydnoraceae hosts typically occur in just two families (Fabaceae, Euphorbiaceae), however, Prosopanche bonacinae has a broad host spectrum of numerous families. Abbreviations: Apo: Apodanthaceae; Bal: Balanophoraceae; Cas: Cassytha; Cus: Cuscuta; Cyn: Cynomoriaceae; Cyt: Cytinaceae; Hyd: Hydnoraceae; Kra: Krameriaceae; Len: Lennoaceae (Boraginaceae sf. Lennooideae); Mit: Mitrastemonaceae; Oro: Orobanchaceae; Raf: Rafflesiaceae; San: Santalales.