Sean Graham


Research Interests

Plant phylogenetics
Plant systematics
Plant evolution
Land plants

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Plant phylogenetics and molecular evolution

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Dissertations completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest dissertations.

Phylogenetics and evolution of monocot mycoheterotrophs and a newly demonstrated lineage of carnivorous monocots (2020)

I used various approaches to investigate mycoheterotrophic and carnivorous monocots, which obtain essential nutrients from soil fungal partners or animal prey, respectively. Fully mycoheterotrophic plants are unable to photosynthesize, and can be difficult to place in plant phylogeny due to substantial morphological modification and elevated substitution rates in all three plant genomes. Mitochondrial genes are expected to be less susceptible to long-branch artefacts in phylogenetic inference than plastid or nuclear genes, as they generally evolve more slowly. I used a phylogenomic approach considering all 37 protein-coding mitochondrial genes to infer the phylogenetic placements of mycoheterotrophic lineages of monocots. I infer that Thismiaceae (excluding Afrothismia) are distantly related to Burmanniaceae, but that fully mycoheterotrophic Afrothismia (Thismiaceae) is the sister group of photosynthetic Taccaceae and core Thismiaceae. The latter finding supports a further independent loss of photosynthesis in Dioscoreales. Scattered distribution of the cox1 intron in distantly related lineages of monocot mycoheterotrophs supports convergent intron gains, potentially consistent with repeated invasions from soil fungal genomes. I demonstrate that Triantha occidentalis (Tofieldiaceae, Alismatales) is a previously overlooked carnivorous lineage with a sticky-trap inflorescence. Field experiments, isotopic data and mixing models demonstrate significant N transfer from prey, with an estimated 68% of leaf N obtained from capture, comparable to levels for co-occurring sundew. Glandular hairs on flowering stems secrete phosphatase, a digestive enzyme seen in other carnivorous plants. Triantha is nearly unique among carnivorous plants in capturing prey on its inflorescence axis close to flowers; however, its glandular hairs capture only small insects. I also studied Triantha phylogeography across its mostly North American range, by surveying 11 plastid-encoded ndh genes from 75 populations. All three North American species are likely monophyletic, although T. occidentalis monophyly requires recognizing T. japonica as a synonym, which is consistent with its nested position in T. occidentalis, as the sister group of populations in Haida Gwaii (Canada). Plastid ndh genes have experienced various degrees of loss or reading frame interruption within T. glutinosa and T. occidentalis, and a strong geographic signal is evident in patterns of ndh gene loss/pseudogenization across the range of T. occidentalis.

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Phylogenomic studies of the monocot sister orders Pandanales and Dioscoreales (2020)

The sister orders Pandanales and Dioscoreales are the last two major clades of monocots that remain to be examined in depth using phylogenomic approaches. Previous studies produced basic phylogenetic outlines for both orders, but left multiple higher-order relationships unresolved, including precise placements of non-photosynthetic mycoheterotrophic lineages. Species-level relationships in the Dioscorea yams, the largest Dioscoreales genus, are also poorly known despite the economic importance of this clade. Here I develop and apply phylogenomic methods to reconstruct the evolutionary histories of Pandanales, Dioscoreales and Dioscorea, using the resulting frameworks to address various phylogenetic and evolutionary hypotheses in each group. I employed a bi-organellar phylogenomic approach to resolve higher-order relationships in Pandanales, with mostly strong support. Mitogenomes are generally slowly evolving, but nevertheless permit inference of well-supported relationships. They also exhibit sporadic order-wide rate accelerations that are decoupled from plastome rate variation. I estimated clade ages to address several biogeographic hypotheses, and uncovered plastome structural variants that may define individual families. In Dioscoreales, I used plastid phylogenomic data and morphology to infer higher-order relationships. The molecular analyses resolve higher-order relationships, but are complicated by extreme substitution rate elevation observed in several mycoheterotrophic lineages. Nevertheless, my analyses confirm the non-monophyly of Burmanniaceae and Dioscoreaceae as currently circumscribed in angiosperm classification schemes. An updated morphological data set supports the local phylogenetic placement of several mycoheterotrophic genera for which plastid data are lacking, and ancestral-state reconstructions predict morphological synapomorphies relevant to the revision of family-level classification schemes. For phylogenomic studies of Dioscorea, I developed a customized bait panel comprising 260 low-to-single-copy nuclear genes. I assessed the utility of the panel with a pilot taxon sampling, supplemented with transcriptome data, that comprises representatives of all major Dioscorea clades, including multiple crop yams. The panel enables resolution of phylogenetic relationships at both deep and recent scales in Dioscorea, mostly with strong support, and provides insights into relationships between crop plants and putative crop wild relatives. Overall, my dissertation offers new insights into a broad diversity of evolutionary questions, made possible by resolution here of recalcitrant phylogenetic relationships in Pandanales, Dioscoreales and the Dioscorea yams.

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Systematics of deep and recent lineages of bryophytes using phylogenomic approaches (2020)

I use organellar phylogenomic approaches to infer overall land-plant phylogeny and higher-order relationships in mosses, liverworts and hornworts, and perform more focused studies of relationships in two bryophyte clades, the granite mosses (Andreaeaceae), and the liverwort genus Herbertus. Using plastid and mitochondrial phylogenomic data sets, I infer conflicts in overall embryophyte relationships across different analyses. These conflicts mask an underlying unrooted tree that is also consistent with most published studies: [(liverworts, mosses), (hornworts, vascular plants)]. Inferred relationships within the major bryophyte clades (mosses, liverworts, hornworts) largely agree across analyses, and between trees inferred from the two organellar genomes. I show that combining genomic and transcriptomic data sources can mislead phylogeny locally for heavily RNA-edited taxa, but that excluding putative edit sites restores cases of unexpected non-monophyly to monophyly. I find that relaxed purifying selection affects multiple plastid genes in a mycoheterotrophic liverwort (Aneura mirabilis) but not a putatively mycoheterotrophic moss, Buxbaumia. Plastid genome structure is nearly invariant across autotrophic bryophytes, but the tufA locus, presumed lost in embryophytes, is unexpectedly retained in several mosses. I reconstruct the broad phylogeny of Andreaeaceae, one of a handful of non-peristomate moss lineages, using a variety of phylogenetic and nuclear phylogenomic data sets and approaches. I infer largely congruent relationships across disparate molecular data sources. These inferences conflict with traditional infrageneric classification, likely reflecting an overreliance on homoplasious morphological characters. I confirm that Andreaea wilsonii is deeply nested in Andreaea, refuting its circumscription as a distinct genus by several authors. I propose an updated infrageneric classification for Andreaea, including three new sections, providing a framework for future systematic studies of the genus. I also use various phylogenetic and nuclear phylogenomic approaches to address species diversity and relationships in Herbertus, a leafy liverwort genus with a complex taxonomic history. My analyses demonstrate an incomplete understanding of species diversity in Herbertus, and reveal widespread misapplication of names due to imperfect morphological species concepts. A reassessment of morphological, ecological, and distributional data in Herbertus, made in light of the new molecular inferences, helps delineate taxa and highlights overlooked species diversity and cryptic species.

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Phylogenomics and Comparative Plastome Analysis of Mycoheterotrophic Plants (2016)

Plastid genomes (plastomes) of fully mycoheterotrophic plants (which obtain nutrition from fungi and have lost photosynthesis) may exhibit accelerated substitution rates, gene losses and structural rearrangements compared to their more stable photosynthetic relatives. Distantly related lineages provide independent data points to study plastome degradation. I used Sanger sequencing to assess the utility of three nonphotosynthetic plastid genes in phylogenetic inference of seven monocot families that include mycoheterotrophic taxa. I also assembled full plastome genomes for multiple mycoheterotrophic monocots, a heterotrophic conifer (Parasitaxus, Podocarpaceae) and autotrophic relatives for comparative analysis. Phylogenomic inferences are robust to different likelihood approaches and often extensive gene loss, are generally congruent with the few-gene analyses, and are insensitive to long branches, in contrast to parsimony. Patterns of gene loss and retention are largely in agreement with hypothesized trajectories, starting with plastid NAD(P)H dehydrogenase, followed by the loss of other photosynthesis-related genes, and ending in gradual loss of transcriptional apparatus and other non-photosynthesis related genes. I observed retention (delayed loss?) of genes encoding subunits of plastid-encoded RNA polymerase (Parasitaxus and some species in Petrosavia, Petrosaviaceae), plastid ATP synthase (Petrosavia, perhaps Parasitaxus in modified form) and Rubisco (Petrosavia), consistent with secondary non-photosynthetic functions of the latter two complexes. Some group IIA introns appear to be retained despite the loss of the plastid intron maturase, matK. Retained open reading frames are generally under strong purifying selection in Sciaphila (Triuridaceae). Genome contraction is the major mode of genome rearrangement, with severe reduction seen in some lineages (e.g., Apteria in Burmanniaceae is reduced to ~16 kb). Some mycoheterotrophs are nearly or completely colinear with autotrophic lineages (Geosiris in Iridaceae, at ~123 kb). Others have multiple minor or major rearrangements, which may be unrelated to the presence or absence of an inverted repeat (IR). Four independent IR losses were observed (in Burmanniaceae, Corsiaceae, Petrosaviaceae and Triuridaceae), an extra IR copy evolved in Campylosiphon (Burmanniaceae), and an entire IR re-evolved in Parasitaxus. Shifts in IR boundaries were also found in all mycoheterotrophs. Within-taxon comparisons (e.g., in Corsiaceae and Petrosavia) also underline that idiosyncratic evolutionary changes may occur following each loss of photosynthesis.

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The phylogeny and evolution of two ancient lineages of aquatic plants (2013)

In my thesis I aim to improve our phylogenetic and evolutionary knowledge of two ancient and distantly related groups of aquatic flowering plants, Hydatellaceae and Alismatales. While the phylogeny of monocots has received fairly intense scrutiny for two decades, some parts of its diversification have been less frequently investigated. One such lineage is the order Alismatales, which defines one of the deepest splits in monocot evolution. Many families of Alismatales are aquatic or semi-aquatic, and they have been implicated in historical discussions of monocot origins. I evaluate inter-familial relationships in the order, considering a suite of 17 plastid genes for 31 Alismatales taxa for all 13 recognized families. This study improves on our understanding of, and confidence in, higher-order Alismatales relationships. I also uncovered convergent gene loss of plastid-encoded subunits for the NADH dehydrogenase complex. I then expand monocot coverage outside Alismatales by including unpublished and newly sequenced data for otherorders. This large-scale sample facilitated a re-evaluation of monocot phylogeny and molecular dating, the latter using 25 fossil constraints. Previously included in the monocot order Poales, Hydatellaceae are a small family of ephemeral aquatics relatively recently found to be the sister group of water lilies (Cabombaceae and Nymphaeaceae). I present the first molecularphylogeny of the family and evaluate aspects of the family's morphological evolution. I show how sexual system shifts are associated with shifts in otherreproductive traits. I also infer a temporal scale for Hydatellaceae diversification using a two-step Bayesian approach. I use the resulting dated tree to address biogeographic patterns and aspects of niche evolution. I show that its "Gondwanan" distribution is the result of long-distance dispersal and not continental rifting, and demonstrate strong phylogenetic niche conservatism in the family. These studies expand our understanding of evolution in Hydatellaceae, and provide a substantial update to our understanding of Alismatales (and more generally monocot) phylogeny and divergence times.

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Effects of adaxial-abaxial signalling on leaf polarity (2012)

The unifying theme of this thesis is adaxial-abaxial or dorsiventral patterning in leaves. The adaxial-abaxial axis sets the thickness of a leaf and without the appropriate juxtaposition of the adaxial and abaxial domains, radialized leaves develop. The underlying genetic mechanisms of the development of these polarity defects started to be elucidated only over the past 20 years in the model Arabidopsis, in particular. I investigated this patterning in a variety of non-model species. Firstly, I investigated the variability of dorsiventral polarity in plants with naturally occurring radialized leaves including Allium, Nepenthes, Krishna fig, Pelargonium, several Cactaceae species, and popREVOLUTA mutant of a poplar hybrid. Subsequent chapters aimed to incorporate morphology and anatomy with molecular genetics in order to elucidate the underlying basis of the phenotype of interest in species that have not been used as model systems for leaf development, including canola and poplar. A novel mutant (lamina epiphylla, lip) was identified in canola, which has adaxialized leaves and leaf-derived organs. Some of the HD-ZIPIII candidate genes were sequenced in canola, but I was unable to determine the location of the LIP mutation. The rest of this thesis focuses on the abaxial greening and unifacial petiole phenotypes seen in some species of poplar that have isobilateral leaves (others in the genus have bifacial leaves). YABBY, KANADI, and HD-ZIPIII genes are some of the major contributors to setting proper adaxial-abaxial polarity and I investigated the relationships of these genes by identifying the orthologs in Arabidopsis, poplar, and eucalyptus (a genus that shares the abaxial greening phenotype with poplar). Further, I studied the species relationships within the genus Populus in order to establish the ancestral state of leaf type. I determined that bifacial leaves are likely derived within the genus. Finally, two poplar species (black cottonwood with bifacial leaves and hybrid aspen with isobilateral leaves) were compared on the basis of morphology, anatomy, and molecular genetics in order to determine the underlying basis of the abaxial greening and unifacial petiole phenotypes in hybrid aspen. I identified a subset of genes that may be involved in determining these phenotypes, but further investigation is needed.

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Molecular phylogenetics of mosses and relatives (2011)

Substantial ambiguities still remain concerning the broad backbone of moss phylogeny. I surveyed 17 slowly evolving plastid genes from representative taxa to reconstruct phylogenetic relationships among the major lineages of mosses in the overall context of land-plant phylogeny. I first designed 78 bryophyte-specific primers and demonstrated that they permit straightforward amplification and sequencing of 14 core genes across a broad range of bryophytes (three of the 17 genes required more effort). In combination, these genes can generate sturdy and well-resolved phylogenetic inferences of higher-order moss phylogeny, with little evidence of conflict among different data partitions or analyses. Liverworts are strongly supported as the sister group of the remaining land plants, and hornworts as sister to vascular plants. Within mosses, besides confirming some previously published findings based on other markers, my results substantiallyimprove support for major branching patterns that were ambiguous before. The monogeneric classes Takakiopsida and Sphagnopsida likely represent the first and second split within moss phylogeny, respectively. However, this result is shown to be sensitive to the strategy used to estimate DNA substitution model parameter values and to different data partitioning methods. Regarding the placement of remaining nonperistomate lineages, the [[[Andreaeobryopsida, Andreaeopsida], Oedipodiopsida], peristomate mosses] arrangement receives moderate to strong support. Among peristomate mosses, relationships among Polytrichopsida, Tetraphidopsida andBryopsida remain unclear, as do the earliest splits within sublcass Bryidae. A Funariidae, [Timmiidae, [Dicranidae, Bryidae]]] arrangement is strongly supported, as are major relationships within subclasses Funariidae and Dicranidae. I also reconstructed the phylogeny of the nonperistomate moss family Andreaeaceae, with a focus on costate taxa, using two complementary sets of plastid markers and taxa. The major subgenera (Andreaea and Chasmocalyx) and sections of Andreaea (Andreaea and Nerviae) are rejected as monophyletic. Well-supported lineages include clades comprising: (1) Andreaea nivalis and A. rigida (northern hemisphere members of subgenus Chasmocalyx) and A. blyttii (section Nerviae); (2) most of the remainder of Nerviae; (3) a mixture of costate and ecostate species from Chasmocalyx, Nerviae,all sampled members of section Andreaea, and subgenus Acroschisma. Relationships among the major lineages, including the root of the family, are all well supported.

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Molecular Phylogenetic Studies of the Vascular Plants (2009)

No abstract available.

Master's Student Supervision

Theses completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest theses.

Plastid phylogenomics and molecular evolution of Thismiaceae (Dioscoreales) (2022)

PREMISE OF THE THESIS: Species in Thismiaceae can no longer photosynthesize, and instead obtain carbon from soil fungi. Here I infer Thismiaceae phylogeny using plastid genome data, and characterize the molecular evolution of this genome. METHODS: I assembled five Thismiaceae plastid genomes from genome skimming data, adding to previously published data for phylogenomic inference. I investigated plastid genome structural changes considering locally colinear blocks (LCBs). I also characterized shifts in selection pressure in retained genes by considering changes in ω, the ratio of non-synonymous to synonymous changes.KEY RESULTS: Thismiaceae experienced two major pulses of gene loss around the early diversification of the family, with subsequent scattered gene losses in descendent lineages. In addition to massive size reduction, plastid genomes experienced occasional inversions and two losses of the inverted repeat (IR) region. Retained plastid genes remain under generally strong purifying selection (ω
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DNA barcoding the vascular plant flora of southern British Columbia (2017)

DNA barcoding is a tool for rapidly identifying species based on short, standardized sequences of DNA, for example in situations where this may be difficult using morphology alone. I assembled a core DNA barcode reference library for southern British Columbia, home to ~54% of the vascular plant species in Canada, using the core plastid barcode loci rbcL and matK, and assessed its utility for identifying species in this region. The library comprises 4,812 sequences obtained from field-collected and herbarium tissue samples, supplemented with sequences downloaded from BOLD and GenBank, with at least one sequence for 75.4% of the vascular plant species occurring below 50°N in British Columbia. Sequence recoverability was significantly higher for rbcL than for matK (93.5% and 80.2%, respectively), and only marginally lower for both markers when using herbarium specimens (90.5% for rbcL and 77.8% for matK), which demonstrates the future feasibility of using museum specimens for completing a southern BC barcode reference library. As a proxy for assessing marker effectiveness, I scored resolution at the level of species and genus using tests of monophyly for Neighbour Joining trees, and performed sequence similarity searches with BLASTn analyses, both for each locus separately and for a dual-locus marker system (rbcL+matK; scored as a cumulative percentage in the BLAST analyses). Ignoring species represented by singleton sequences, the highest overall level of discrimination (66.9% of species and 91.6% of genera) was achieved for BLASTn analysis of rbcL+matK together. This work represents a significant contribution to a nation-wide barcode database, and provides a preliminary platform for ecological and other applications requiring species identification, where traditional methods are not feasible.

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Plastid genome evolution in partially and fully mycoheterotrophic eudicots (2016)

Plastid-genome evolution following photosynthesis loss is characterized by substantial change, contrasting with strong conservation in most photosynthetic land plants. Common features of reduced plastid genomes across diverse heterotrophic lineages point to a predictable trajectory of genome degradation, but this has been only partly tested. Here I document the molecular evolution of plastid genomes belonging to several mycoheterotroph lineages in Ericaceae, Gentianaceae and Polygalaceae, which include several independent origins of mycoheterotrophy in eudicot angiosperms that span different time scales since photosynthesis loss. I used next-generation and Sanger sequencing techniques to assemble complete plastomes or gene sets for comparative analyses of gene content and genome structure, and phylogenomic inference. I also sequenced several partially mycoheterotrophic and fully autotrophic relatives. Patterns of gene loss in mycoheterotroph plastomes are generally consistent with a previously hypothesized trajectory of change, starting with the loss of plastid NAD(P)H dehydrogenase before full loss of photosynthesis, and ending (here) with substantial reduction in genes involved in the translation apparatus and other nonphotosynthetic functions. Several retentions (delayed losses) of subunit genes for plastid-encoded polymerase, plastid ATP synthase and Rubisco are also consistent with hypothesized secondary (nonphotosynthetic) functions for these complexes. Two within-genus comparisons (for Epirixanthes in Polygalaceae and Voyria in Gentianaceae) demonstrate substantially different levels of genome degradation, consistent with heterogeneity in rates of genome change after a given origin of full mycoheterotrophy. Mycoheterotrophs in two families (Ericaceae, Polygalaceae) have extensive genome rearrangement compared to most land plants, contrasting with near colinearity in mycoheterotrophic members of Gentianaceae (despite sometimes extensive genome reduction in the latter). However, these contrasting patterns are apparently not associated with transitions to mycoheterotrophy, as photosynthetic relatives in Ericaceae and Polygalaceae are also substantially rearranged—or with inverted repeat loss (evident in Epirixanthes pallida, Polygalaceae), as autotrophic Polygala retains its inverted repeats. Phylogenomic inferences of core eudicot phylogeny made using the retained genes are generally well supported and robust to a variety of phylogenetic approaches, and are also congruent with recent phylogenetic studies in each mycoheterotrophic family.

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Phylogenetics and molecular evolution of Alismatales based on whole plastid genomes (2015)

The order Alismatales is a mostly aquatic group of monocots that displays substantial morphological and life history diversity, including the seagrasses, the only land plants that have re-colonized marine environments. Past phylogenetic studies of the order have either considered a single gene with dense taxonomic sampling, or several genes with thinner sampling. Despite substantial progress based on these studies, multiple phylogenetic uncertainties still remain concerning higher-order phylogenetic relationships. To address these issues, I completed a near-genus level sampling of the core alismatid families and the phylogenetically isolated family Tofieldiaceae, adding these new data to published sequences of Araceae and other monocots, eudicots and ANITA-grade angiosperms. I recovered whole plastid genomes (plastid gene sets representing up to 83 genes per taxa) and analyzed them using maximum likelihood and parsimony approaches. I recovered a well supported phylogenetic backbone for most of the order, with all families supported as monophyletic, and with strong support for most inter- and intrafamilial relationships. A major exception is the relative arrangement of Araceae, core alismatids and Tofieldiaceae; although most analyses recovered Tofieldiaceae as the sister-group of the rest of the order, this result was not well supported. Different partitioning schemes used in the likelihood analyses had little effect on patterns of clade support across the order, and the parsimony and likelihood results were generally highly congruent. I also used the inferred phylogeny of Alismatales to study the loss of the mostly plastid-encoded NADH dehydrogenase enzyme complex in the order. This enzyme is hypothesized to be involved in mitigating photooxidative stress by inducing chlororespiration. The inclusion or exclusion of ndh pseudogenes had little impact on the main phylogenetic results. Previous work hypothesized three independent losses/pseudogenization events within the core alismatids, which I confirmed here. I also inferred an additional loss in Tofieldiaceae, the first example in unsubmerged species of Alismatales. The repeated loss of plastid NADH dehydrogenase may spur future research into the physiological bases of the loss.

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Using a low-copy nuclear gene (phosphoglycerate kinase: PGK) to explore the phylogeny of the aquatic plant family Hydatellaceae (Nymphaeales) (2014)

Hydatellaceae are a small aquatic family of 12 species related to water lilies, part of the ANITA grade of angiosperms. Our current understanding of phylogenetic relationships in the family comes from several plastid genes and nuclear ITS data. These data sets are generally highly congruent, and lend support to the monophyly of multiple species. However, the published nuclear ITS tree was unrooted (outgroups were too distant to align), and there were several minor phylogenetic conflicts between plastid and ITS gene trees for three closely related species, Trithuria bibracteata, T. occidentalis, and T. submersa; two of these species were also not reciprocally monophyletic in individual gene trees. The position of T. occidentalis was also based on very limited plastid data, and there was no molecular evidence to link staminate and pistillate individuals in this species. To further clarify phylogenetic relationships and species boundaries, I recovered two copies of nuclear-encoded phosphoglycerate kinase (PGK) gene from taxa in Hydatellaceae and several water lilies. I reconstructed the history of the PGK duplication in angiosperms as a whole. I also added plastid data from additional populations of several species, and estimated the dated species tree using a Bayesian multispecies coalescent approach to reconcile different gene trees. The angiosperm-level PGK gene tree indicated that the duplication of PGK gene may have happened around the origin of angiosperms. The root of Hydatellaceae implied by concatenated nuclear PGK matches that inferred from plastid data. Trithuria occidentalis is clearly placed in sect. Trithuria, and staminate and pistillate individuals of this species are linked together using new evidence from the plastid and PGK genes. Phylogenetic relationships inferred using each PGK copy are consistent with the sectional relationships inferred using plastid and ITS data, with less sharply defined species boundaries. I also explore the possibility here that some of the incongruence that I observed between individual genes trees and in inferred species trees is a consequence of additional minor gene duplications or polyploidization/introgression events.

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