Quentin Charles Cronk


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Doctoral Student Supervision (Jan 2008 - Nov 2020)
Genetic population structure, patterns of genetic variation, and patterns of phenotypic leaf variation among peripheral and core populations of the mangrove species Avicennia marina (Forsk.) Vierh. (Acanthaceae) on the red sea, Saudi Arabia (2019)

This study utilized both of leaf dimension measurements (leaf area, length, maximal width, and the ratio of length: width) and 12 microsatellite loci screened across 315 samples of the entomophilous mangrove species Avicennia marina (Forsk.) Vierh. The samples collected from 9 sites along the Saudi Arabian Red Sea coastline with an estimated sampling range of 1,345 kilometres. The study objectives were to examine the genetic diversity, population structure, and the field observed phenotypic leaf variation, and to inspect the influence of the distribution limit on the genetic compositions and the phenotypic leaf traits variation. The 12 loci detected a total of 89 alleles with an average allelic diversity of 7.42. Observed heterozygosity (Hₒ) was close to expected heterozygosities (Hₑ) for most sites, and the average (Hₒ) was 0.298. The levels of inbreeding ranged from negative 0.044 to positive 0.126, with an average inbreeding coefficient of 0.012. The component of variation among populations were (25%, 34%) (p
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Adaptive introgression from Populus balsamifera (balsam poplar) in P. trichocarpa (black cottonwood) (2017)

Hybridization is a widespread phenomenon that has shaped the genome of many lineages. In natural hybrid zones, back-crossing of early-generation hybrids over subsequent generations can result in introgression which can introduce adaptive genetic variation. Populus has emerged as a model genus for population genomic studies of adaptation due to porous species barriers and a wealth of genomic resources available. Populus trichocarpa and P. balsamifera are sibling poplar species ecologically divergent and adapted to strongly contrasting environments. In this thesis, I provide evidence for adaptive introgression in P. trichocarpa and P. balsamifera, by implementing local ancestry analyses together with functional, phenotypic and selection tests. Based on a local ancestry analysis across the whole genome, I detected asymmetric patterns of introgression with stronger signals of introgression from P. balsamifera to P. trichocarpa than vice versa. There was no overlap between the introgressed regions in P. trichocarpa compared to those in P. balsamifera or the enriched GO and Pfam terms in the introgressed regions. In admixed P. trichocarpa individuals, candidate regions for adaptive introgression showed strong signals of selection and were enriched for genes that may play crucial roles for survival and adaptation. These analyses also revealed overrepresentation of P. balsamifera introgression in subtelomeric regions and possible protection of the sex-determining regions from interspecific gene flow. An admixture mapping analysis and phenotypic tests provided strong support that introgressive hybridization is a driver of clinal adaptation in P. trichocarpa and suggest that the northern range extension of P. trichocarpa depends, at least in part, on introgression of alleles from P. balsamifera. A number of genomic regions showing unusually high levels of P. balsamifera introgression were significantly associated with putatively adaptive trait combinations, in particular, regions on chromosome 9 and chromosome 15. Overall, these results contribute to our understanding of introgression as a source of genetic variation associated with adaptive characters that may allow improved survival in new environments. To my knowledge, this is the first fine-scale study on natural hybrids of tree species with such a comprehensive view of the effects of admixture in adaptation.

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The molecular evolution of floral colour shifts in Lathyrus L. (Fabaceae) (2016)

In this thesis, I used Lathyrus to study floral colour evolution. My work builds on that of pioneer geneticists who used the sweet pea (Lathyrus odoratus) for research in early 20th century England. They used the rich horticultural resource of inbred cultivars for genetic study. More recently, studies on flavonoid biochemistry and the phylogenetics of Lathyrus lend tools to place the colour shifts in an evolutionary and molecular context. In chapter 2, I show that the A1 locus is a missense mutation (332 G/A) in the substrate recognition site (SRS1) of flavonoid 3’,5’-hydroxylase (F3’5’H) and is associated with the pink mutant cultivar ‘Painted Lady’ (‘PL’). This single base pair substitution in the mutant F3’5’H is speculated to toggle the enzyme from primary F3’5’H activity to a relatively efficient F3’H, as shown in a heterologous transformation in Arabidopsis PAP1D (a mutant line that produces anthocyanin constitutively). In chapter 3, I constructed a multi-species coalescent tree using Bayesian inference and reconstructed the ancestral states for floral colour, life history trait (perennial or annual) and floral pattern. The ancestral states for Lathyrus are anthocyanin rich (AR), annual and concolourous. However, no correlation was found between the life history trait (which is linked to breeding systems) and the loss of anthocyanin colour in the petal, when corrected for phylogenetic independence. This suggests that in Lathyrus, autogamous species are as colourful as allogamous ones even though the latter are expected to need greater floral display. In chapter 4, I found that the lack of expression in dihydroflavonol reductase (DFR) was associated with a white mutant cultivar ‘Mrs Collier’ (‘MC’) of L. odoratus via a trans-regulatory machinery. Two transcription factors, the sweet pea orthologues of AN2 (MYB) and AN1 (bHLH) were also not expressed although neither was associated with the white phenotype in an F2-cosegregation analysis. This DFR silencing was also observed in another white mutant of the domesticated grass pea (L. sativus). In contrast, when unpigmented wild species originate under natural selection, DFR expression, if at all affected, is lowered rather than fully silenced, likely due to pleiotropic effects.

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Investigations into plant genome evolution using massive parallel sequencing (2014)

The advancements of various massively parallel sequencing (MPS) methods in the last five years have enabled researchers to tackle biological problems that until recently seemed intractable. One of the most widely used MPS methods comes from Illumina®, which combines short and accurate sequencing reads with high throughput. Data generated using Illumina sequencing is used in every chapter of this thesis to characterize patterns of genome evolution using phylogenetic approaches in various plant genera. The thesis is focused on three main aspects of plant genome evolution: transposable elements (chapter 2), polyploidy (chapters 3 and 4) and plastid genomes (chapters 5 and 6). In every chapter phylogenetic hypotheses are generated from sequences assembled from Illumina reads, which I use to frame my research questions. In chapter 2 I investigated intra- and interspecific patterns of transposable element (TE) abundance in Theobroma cacao and related species. I found that reference based mapping of short sequencing reads works well to characterize TEs within the same species but is not reliable for interspecific comparison. In chapter 3 I used Illumina sequenced transcriptomes of 11 flax species, to investigate the presence of paleopolyploidy event within the genus. I discovered a previously unknown paleopolyploidy event, occurring 23 – 42 million years ago. In chapter 4 I used low coverage Illumina whole genome sequencing to test a hypothesis regarding the allopolyploid origin of a North-American Lathyrus species, L. venosus. I conclude that L. venosus is not of hybrid origin, since no incongruencies were detected between nuclear and plastid phylogenies. In chapter 5 I pinpointed the evolutionary origin of highly repetitive plastid genomes that are known to exist within the clover genus (Trifolium). I discovered that the repetitive plastomes are restricted to a single clade within Trifolium, which I estimated to be 12.4 – 13.8 million years old. In chapter 6 I investigated the pattern of gene rearrangements in the IRLC clade of legumes. While plastomes are highly rearranged in this group, I characterized certain highly conserved gene blocks that have not been rearranged internally, and argue that these blocks may represent the fundamental gene regulatory organization of the plastid.

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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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Investigation of the genomics of gender regulation in populus trichocarpa (2012)

This thesis reports the findings of four projects conducted to study the genomics of gender regulation in Populus trichocarpa. Sex-linked markers previously discovered in Salix vimilanis were tested to determine if they were also sex-linked in other Salix species and P. trichocarpa. It was found that the DNA sequence of the SCAR 354 marker, and its position at the 5’ end of a gene encoding an Ssu72-like protein, was conserved with some SFP variability in species of Salix and P. trichocarpa. While this marker may be useful for phylogenetic or population studies in Salix, this marker was not sex-linked in the species investigated in this study. An investigation of genes located on the telomeric end of chromosome 19, the putative sex chromosome in P. trichocarpa, was conducted to look for gender-biased SNPs that would indicate recombination suppression in the region on a sex locus. A large variability in the number of SNPs was observed in the gene sequences studied, but no SNPs that segregated with gender were discovered so a genetic marker that could be used to sex P. trichocarpa individuals of unknown gender could not be developed. Using a microarray approach, gender-biased gene-expression was studied in leaf tissue of P. trichocarpa. While some gender-biased gene-expression was observed in vegetative tissues the differences observed were statistically insignificant due to biological variation in the samples tested, the small sample size used in this study, and changes in the genome annotation between version 1.1 and 2.0 of the poplar genome. This study could not verify the microarray results using rtPCR in a larger sample of male and female leaf tissue. MADS-box genes involved in floral development were identified as having gender-biased gene-expression using a microarray approach. Thirteen putative MADS-box genes that showed gender-biased expression in male and female inflorescences were discovered. Novel expression patterns for nine floral MADS-box genes were identified with this microarray data, and the expression patterns of three of these genes were investigated in further detail using reverse-transcription PCR.

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Evolution of bird pollination in Macaronesian Lotus (Leguminosae) (2011)

In order to understand the evolutionary transition from bee pollination (melittophily) to bird pollination (ornithophily), I studied a group of Lotus from Macaronesia. First, I provided a combined phylogenetic framework using nuclear and plastid genes, where I showed that the morphological features adapted to opportunistic passerine birds in Tenerife and La Palma are derived and evolved recently within the last 1.2 Ma in four species. I also identified Lotus sessilifolius as the most likely closely related species with melittophily.I showed that L. sessilifolius and the clade where this syndrome evolved had a pre-adaptation to produce a color change to red flowers (and the associated anthocyanidin pigment, cyanidin) as a possible strategy to increase bee foraging efficiency. The transition from yellow to red flowers in this group required only a redirection in the flux of pigment production and a modification in the proportions of flavonols and anthocyanidins, especially within the cyanidin branch.I also found that petal micromorphology is highly modified between the two syndromes. I found that ornithophilous flowers lack the typical papillose conical cells, which are distributed in the exposed sides of the petals in bee-pollinated flowers. This reduction of conical cells is associated with an early down-regulation of a dorsal identity gene in legumes, LjCYC2. Bird-pollinated flowers also have a higher proportion of tabular rugose cells in all three types of petals in comparison with the bee-pollinated species. The increase of this epidermal type is associated with an up-regulation of LjCYC3, a lateral petal identity gene, during early stages of flower development in the dorsal and lateral petals. Lotus sessilifolius also seems to have this early expression in comparison with other bee-pollinated species. All this evidence suggests that the transition from bee to bird pollination in this group required only heterochronic modifications of the genes involved in flower color and petal micromorphology. It seems that ornithophily in Lotus evolved within a group which has at least two pre-adaptations, production of pigments required for red colors and an increase in the amount of tabular rugose cells, which likely facilitated the evolution of phenotypes associated with this pollination syndrome in the Canary Islands.

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Master's Student Supervision (2010 - 2018)
Transcriptomics of post-anthesis colour change in Lotus (2017)

Post-anthesis colour change (PACC) is widely thought to be an adaptation to signal floral viability to pollinators, and may be a developmental pre-pattern for bird pollination in Lotus. Lotus filicaulis and Lotus sessilifolius are insect-pollinated herbaceous legumes with flowers that open yellow, shift to orange and finally, red. This thesis examines the ecological and molecular basis for floral colour change in these Lotus species. L. filicaulis was cultivated in a glasshouse from which pollinating insects (bees) were excluded, and the rate of colour change was recorded in both unpollinated and manually pollinated flowers. Unpollinated flowers from both the yellow stage and red stage were sampled for sequencing. The transcriptomes of L. filicaulis and L. sessilifolius of both colour stages were analyzed for differentially expressed genes and enriched ontologies. Pollination significantly accelerates PACC in L. filicaulis, consistent with the hypothesis that PACC increases pollination efficiency by directing pollinators to unpollinated flowers. RNA-seq results show the synchronized upregulation of the entire cyanidin biosynthesis pathway in the red stage of PACC of both Lotus species – possibly at the expense of adjacent pathways competing for the same substrate. This thesis is the foundation for understanding the molecular evolution of PACC in Lotus and will be useful in testing the hypothesis that PACC is a preadaptation to bird pollination in Lotus.

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