Evolution of Epiphytism and Fruit Traits Act Unevenly on the Diversification of the Species-Rich Genus Peperomia (Piperaceae)

The species-rich genus Peperomia (Black Pepper relatives) is the only genus among early diverging angiosperms where epiphytism evolved. The majority of fruits of Peperomia release sticky secretions or exhibit hook-shaped appendages indicative of epizoochorous dispersal, which is in contrast to other flowering plants, where epiphytes are generally characterized by fruit morphological adaptations for anemochory or endozoochory. We investigate fruit characters using Cryo-SEM. Comparative phylogenetic analyses are applied for the first time to include life form and fruit character information to study diversification in Peperomia. Likelihood ratio tests uncover correlated character evolution. We demonstrate that diversification within Peperomia is not homogenous across its phylogeny, and that net diversification rates increase by twofold within the most species-rich subgenus. In contrast to former land plant studies that provide general evidence for increased diversification in epiphytic lineages, we demonstrate that the evolution of epiphytism within Peperomia predates the diversification shift. An epiphytic-dependent diversification is only observed for the background phylogeny. An elevated frequency of life form transitions between epiphytes and terrestrials and thus evolutionary flexibility of life forms is uncovered to coincide with the diversification shift. The evolution of fruits showing dispersal related structures is key to diversification in the foreground region of the phylogeny and postdates the evolution of epiphytism. We conclude that the success of Peperomia, measured in species numbers, is likely the result of enhanced vertical and horizontal dispersal ability and life form flexibility but not the evolution of epiphytism itself

Stem biomechanics of the giant moss Dendroligotrichum dendroides and their significance for growth form diversity in mosses

ACL-11-57International audienceThe giant moss Dendroligotrichum dendroides s.l. grows as self-supporting plants up to 40 cm in height in forest habitats in Chile and New Zealand. This moss represents one of the tallest self-supporting bryophytes. Biomechanical tests indicate that the stems can develop a high degree of stiffness (Young's modulus) via a dense hypodermal sterome that is comparable with that of woody stems of vascular plants. A comparison with mechanical properties of other terrestrial and aquatic mosses indicates that different moss growth and life forms can produce very different mechanical architectures. Values of stem stiffness can vary between different growth forms of mosses to a comparable extent to that observed among diverse growth forms of vascular plants. Plants varying profoundly in overall size, development, and phylogenetic position nevertheless appear to develop comparable mechanical adaptations and growth forms in response to certain environmental condition

Single-Copy Nuclear Genes Place Haustorial Hydnoraceae within Piperales and Reveal a Cretaceous Origin of Multiple Parasitic Angiosperm Lineages

<div><p>Extreme haustorial parasites have long captured the interest of naturalists and scientists with their greatly reduced and highly specialized morphology. Along with the reduction or loss of photosynthesis, the plastid genome often decays as photosynthetic genes are released from selective constraint. This makes it challenging to use traditional plastid genes for parasitic plant phylogenetics, and has driven the search for alternative phylogenetic and molecular evolutionary markers. Thus, evolutionary studies, such as molecular clock-based age estimates, are not yet available for all parasitic lineages. In the present study, we extracted 14 nuclear single copy genes (nSCG) from Illumina transcriptome data from one of the “strangest plants in the world”, <i>Hydnora visseri</i> (Hydnoraceae). A ∼15,000 character molecular dataset, based on all three genomic compartments, shows the utility of nSCG for reconstructing phylogenetic relationships in parasitic lineages. A relaxed molecular clock approach with the same multi-locus dataset, revealed an ancient age of ∼91 MYA for Hydnoraceae. We then estimated the stem ages of all independently originated parasitic angiosperm lineages using a published dataset, which also revealed a Cretaceous origin for Balanophoraceae, Cynomoriaceae and Apodanthaceae. With the exception of Santalales, older parasite lineages tend to be more specialized with respect to trophic level and have lower species diversity. We thus propose the “temporal specialization hypothesis” (TSH) implementing multiple independent specialization processes over time during parasitic angiosperm evolution.</p></div

The emergent trilobed flower of <i>Hydnora visseri.</i>

<p>This photograph was taken at the type locality (Farm Namuskluft) in the Richtersveld region of southwestern Namibia. The host of <i>H. visseri</i> is <i>Euphorbia gummifera</i> at the type location (host not pictured).</p

Phylogenetic origin of Hydnoraceae within photosynthetic Piperales.

<p>To compare the performance of individual marker combinations, separate analyses were run and are summarized here. The plastid <i>rbcL</i> and <i>atpB</i> 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 (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0079204#pone-0079204-g002" target="_blank">Figure 2D</a>) 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 (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0079204#pone.0079204.s001" target="_blank">Figure S1E–F</a>).</p

The “temporal specialization hypothesis” (TSH) postulates increasing specialization during the evolution of parasitism in plants.

<p>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. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0079204#pone.0079204-Westwood1" target="_blank">[51]</a>). 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 <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0079204#pone.0079204-Nickrent5" target="_blank">[36]</a>. 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, <i>Prosopanche bonacinae</i> has a broad host spectrum of numerous families. Abbreviations: Apo: Apodanthaceae; Bal: Balanophoraceae; Cas: <i>Cassytha</i>; Cus: <i>Cuscuta</i>; Cyn: Cynomoriaceae; Cyt: Cytinaceae; Hyd: Hydnoraceae; Kra: Krameriaceae; Len: Lennoaceae (Boraginaceae sf. Lennooideae); Mit: Mitrastemonaceae; Oro: Orobanchaceae; Raf: Rafflesiaceae; San: Santalales.</p

Relative substitution rates of nuclear single copy genes (nSCG) are elevated.

<p>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 (<a href="http://bioinfweb.info/Software/GRate" target="_blank">http://bioinfweb.info/Software/GRate</a>) for different Piperales lineages using Canellales (<i>Canella</i>) as the reference and all other sampled taxa as outgroups.</p