Convergence in carnivorous pitcher plants reveals a mechanism for composite trait evolution.

Composite traits involve multiple components that, only when combined, gain a new synergistic function. Thus, how they evolve remains a puzzle. We combined field experiments, microscopy, chemical analyses, and laser Doppler vibrometry with comparative phylogenetic analyses to show that two carnivorous pitcher plant species independently evolved similar adaptations in three distinct traits to acquire a new, composite trapping mechanism. Comparative analyses suggest that this new trait arose convergently through "spontaneous coincidence" of the required trait combination, rather than directional selection in the component traits. Our results indicate a plausible mechanism for composite trait evolution and highlight the importance of stochastic phenotypic variation as a facilitator of evolutionary novelty

The biosynthetic mechanisms behind mid-chain functional groups of plant cuticular waxes

The cuticles covering aerial organs of most plants contain a complex mixture of fatty acid-derived waxes, with various chain lengths and diverse functional groups. These waxes can form crystals which then dictate the physical properties of the surface, by accumulating either ubiquitous compounds or specialty components that are restricted to certain taxa. Relatively little is known about the biosynthesis of the specialty compounds, and whether unrelated species utilize the same mechanisms to form them. However, specialty wax biosynthesis must be elucidated to understand the formation of wax crystals and, therefore, the mechanisms underlying plant protection against drought and other stresses. The goal of my thesis is to further our understanding of the biosynthesis of specialty compounds ketones and β-diketones. Specifically, I aimed to: (i) carry out in-depth wax analyses of co-occurring compound classes, homologs and isomers with implications for possible biosynthetic mechanisms; (ii) identify and characterize enzymes involved in β-diketone formation based on comparative analysis of β-diketones and related compounds in closely and remotely related plant species. This work was done on species that were confirmed or suspected to comprise ketones and β-diketones. Furthermore, the species were chosen for their importance as food crops (Allium fistulosum, Triticum aestivum), ornamental plants (Dianthus species) or biofuels (Panicum virgatum). To achieve the first goal, I analyzed and compared the wax compositions of Allium fistulosum wild type and a wax-deficient mutant, which allowed for elucidation of the mechanism for ketone and ketol formation by carbon chain elongation, in contrast to the previously described hydroxylation mechanism. For the waxes of Dianthus species, I found characteristic chain length profiles that had implications for the mechanisms underlying β-diketone production. To achieve the second goal, I carried out wax analyses of several species across Poaceae subfamilies to investigate the ubiquity of their biosynthetic mechanisms. This was followed by characterization and functionalization of the main enzymes involved in β-diketone production. Overall, this work highlights the importance of understating the underlying mechanisms behind mid-chain functional compound production and the effects those mechanisms have on chain-length, deposition and therefore crystal formation.Science, Faculty ofChemistry, Department ofGraduat

Raw data and Matlab code for: Convergence in carnivorous pitcher plants reveals a mechanism for composite trait evolution

<p>Composite traits involve multiple components that, only when combined, gain a new synergistic function. Thus, how they evolve remains a puzzle. We combined field experiments, microscopy, chemical analyses and laser Doppler vibrometry with comparative phylogenetic analyses to show that two carnivorous <em>Nepenthes</em> pitcher plant species convergently evolved identical adaptations in three distinct traits to acquire a new, composite trapping mechanism. Comparative analyses suggest that this new trait arose convergently via 'spontaneous coincidence' of the required trait combination, rather than directional selection in the component traits. Our results indicate a plausible mechanism for composite trait evolution and highlight the importance of stochastic phenotypic variation as a facilitator of evolutionary novelty.</p><p>No specialist software is required. Data files are in .csv format. Images are in .tif format. Video files are in .avi format.</p><p>Funding provided by: UK Research and Innovation<br>Crossref Funder Registry ID: https://ror.org/001aqnf71<br>Award Number: EP/X026868/1</p><p>Funding provided by: Natural Sciences and Engineering Research Council<br>Crossref Funder Registry ID: https://ror.org/01h531d29<br>Award Number: 2018-04909</p><p>Funding provided by: Royal Society<br>Crossref Funder Registry ID: https://ror.org/03wnrjx87<br>Award Number: UF\R\221028</p><p>Funding provided by: Royal Commission for the Exhibition of 1851<br>Crossref Funder Registry ID: https://ror.org/05fdb2817<br>Award Number: Fellowship</p><p>Funding provided by: National Science Foundation<br>Crossref Funder Registry ID: https://ror.org/021nxhr62<br>Award Number: IOS 1812037</p><p>Funding provided by: Leverhulme Trust<br>Crossref Funder Registry ID: https://ror.org/012mzw131<br>Award Number: RPG-2019-323</p><p>Funding provided by: Natural Environment Research Council<br>Crossref Funder Registry ID: https://ror.org/02b5d8509<br>Award Number: NE/S014470/1</p><p>Funding provided by: Royal Society<br>Crossref Funder Registry ID: https://ror.org/03wnrjx87<br>Award Number: URF/R1/191033</p><p>Funding provided by: Royal Society<br>Crossref Funder Registry ID: https://ror.org/03wnrjx87<br>Award Number: UF150138</p><p>Data were collected from 55 <em>Nepenthes </em>pitcher plant species from Botanical collections in the UK, Germany and Switzerland, as well as from two species (<em>N. gracilis</em> and <em>N. pervillei</em>) from natural populations in Borneo and the Seychelles. Fotos and high-speed videos were used to assess two macromorphological traits: (1) lid orientation (deviation from horizontal in °), and (2) lid loading/impact response (qualitatively from Fotos, and quantitatively from high-speed video recordings). Laser Doppler vibrometry was used for detailed analysis of lid oscillations after a drop impact on the lid. Scanning electron microscopy was used to assess surface microtopography (images are shown in the article supplementary material, Figures S1 and S2, and are not included in this dataset). Gas-chromatography mass-spectrometry was used to investigate the chemical composition of surface waxes. For detailed descriptions of the experimental methods and sampling techniques see online supplementary material, Materials and Methods.</p&gt

Raw data and Matlab code for: Convergence in carnivorous pitcher plants reveals a mechanism for composite trait evolution

AbstractComposite traits involve multiple components that, only when combined, gain a new synergistic function. Thus, how they evolve remains a puzzle. We combined field experiments, microscopy, chemical analyses and laser Doppler vibrometry with comparative phylogenetic analyses to show that two carnivorous Nepenthes pitcher plant species convergently evolved identical adaptations in three distinct traits to acquire a new, composite trapping mechanism. Comparative analyses suggest that this new trait arose convergently via ‘spontaneous coincidence’ of the required trait combination, rather than directional selection in the component traits. Our results indicate a plausible mechanism for composite trait evolution and highlight the importance of stochastic phenotypic variation as a facilitator of evolutionary novelty

Raw data and Matlab code for: Convergence in carnivorous pitcher plants reveals a mechanism for composite trait evolution

Composite traits involve multiple components that, only when combined, gain a new synergistic function. Thus, how they evolve remains a puzzle. We combined field experiments, microscopy, chemical analyses and laser Doppler vibrometry with comparative phylogenetic analyses to show that two carnivorous Nepenthes pitcher plant species convergently evolved identical adaptations in three distinct traits to acquire a new, composite trapping mechanism. Comparative analyses suggest that this new trait arose convergently via ‘spontaneous coincidence’ of the required trait combination, rather than directional selection in the component traits. Our results indicate a plausible mechanism for composite trait evolution and highlight the importance of stochastic phenotypic variation as a facilitator of evolutionary novelty