Brian Leander

Professor

Research Interests

Evolutionary morphology
Marine invertebrate zoology
Evolutionary protistology
Species discovery
Phylogenetic biology
Comparative organismal biology
Marine biodiversity

Relevant Degree Programs

 

Research Methodology

Marine field collections
Electron Microscopy
Confocal microscopy
Molecular phylogenetics
Character evolution
Systematics

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Graduate Student Supervision

Doctoral Student Supervision (Jan 2008 - May 2019)
Evolution of complex organelles in dinoflagellates (2016)

Dinoflagellates are an abundant and diverse group of aquatic eukaryotes, with members that have photosynthetic, heterotrophic, or mixotrophic life strategies, as well as a number of unique cytological features. My thesis focuses on two groups of closely related dinoflagellates: polykrikoids and warnowiids. Both include heterotrophic as well as plastid-bearing members, though the number of times photosynthesis has been lost (or gained) in each group is unclear, and the presence and provenance of plastids in some species (e.g., Nematodinium sp. and Polykrikos lebouriae) have been debated. Polykrikoids and warnowiids also contain some of the most complex subcellular structures described--such as nematocysts and, in warnowiids, eye-like ocelloids. Yet these groups are rare in nature and uncultivated, and as such, the origins of their complex organelles are unclear. For my thesis, I modified existing techniques for use on single-cell environmental isolates, and applied these techniques to wild polykrikoid and warnowiid cells. By exploiting the common splice leader sequence found on dinoflagellate transcripts, I was able to amplify a single-cell transcriptome from Polykrikos lebouriae—a dinoflagellate with aberrant plastids. Coupled with single-cell genomics using multiple displacement amplification (MDA), I demonstrated that Polykrikos lebouriae has retained peridinin-type plastids, while photosynthesis has been lost in multiple other polykrikoid species independently. Using MDA and single-cell transmission electron microscopy, I also determined that the eye-like ocelloid of Nematodinium sp. is made in part from a peridinin plastid, and also from mitochondria. Specifically, single-cell focused ion beam scanning electron microscopy (FIB-SEM) allowed me to demonstrate that a retina-like portion of the ocelloid is a small part of a much larger peridinin-plastid that ramifies throughout the Nematodinium cell. Lastly, I investigated the evolution of nematocysts in Polykrikos spp. and Nematodinium sp. using a combination of transcriptomics, TEM, SEM, and FIB-SEM, and inferred that “nematocysts” in these groups evolved independently from those in cnidarians. Thus, nematocyst-like extrusive organelles appear to have evolved multiple times in eukaryotes. The data presented in this thesis show how extreme subcellular complexity has evolved in dinoflagellates through both endosymbiotic and autogenous origins.

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Species discovery and evolutionary history of marine gregarine apicomplexans (2014)

Gregarine apicomplexans are a diverse but poorly understood group of single-celled parasites infecting a wide range of invertebrates in marine, freshwater and terrestrial environments. My thesis focuses on marine gregarines. Gregarines from marine hosts are unique because some (archigregarines) have maintained a set of pleisiomorphic characteristics from the ancestor of gregarines and apicomplexans alike. Other lineages of marine gregarines (eugregarines) are thought to have been modified from this archigregarine morphotype, and represent a wide-range of diversity with regard to general morphology, motility, and feeding strategies. My work has broadly applied molecular phylogenetics to novel species of marine gregarines from areas around British Columbia, Canada and Okinawa, Japan, with the goal of placing the evolution of gregarines in a molecular phylogenetic context. I amplified mainly SSU rDNA from a distinct life history stage (trophozoites), and coupled that with morphological data I gathered from light, confocal, as well as electron microscopy. Although my work was unable to resolve deep phylogenetic relationships among gregarines (and apicomplexans), this work did improve our understanding of evolution within gregarines. With the discovery of Veloxidium leptosynaptae from the gut of an echinoderm in Bamfield, British Columbia, and Surculinium glossobalanae from a hemichordate in Okinawa, I was able to show the paraphyly of the archigregarine morphotype, and polyphyly of other gregarine lineages, including some groups of neogregarines and eugregarines in terrestrial and freshwater environments. With the description Polyplicarium, my work uncovered and identified an ambiguous environmental sequence clade and, along with other work on Selenidium, was able to show that SSU rDNA can be reliably isolated from single cells as a method for delimiting closely related or morphologically similar species. In my final data chapter, I conducted an in-depth study on the morphology and molecular phylogenetic relationships between two sister species from the same host, Selenidium terebellae, and a newly discovered species, Selenidium melitzanae. Results from this data gave me the first opportunity to compare character evolution and niche partitioning among closely related gregarines, and provided another example of convergence of the eugregarine morphotype.

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Contributions to the ultrastructural diversity and molecular phylogeny of phagotrophic euglenids and their episymbionts (2012)

The Euglenida is a diverse group of single celled eukaryotes with modes of nutrition that include phagotrophy, osmotrophy, and phototrophy. Phototrophic members of the group have attracted the most attention from previous researchers, and some species (e.g., Euglena gracilis) have become models in cell biology research. Phagotrophic euglenids, by contrast, are difficult to cultivate and manipulate so are severely underrepresented in culture collections, comparative ultrastructural studies, and molecular phylogenetic studies. Species discovery and the comparative ultrastructure of phagotrophic euglenids within a phylogenetic context were the main aims of this thesis. These data are essential for a comprehensive knowledge of the overall diversity and evolutionary history of euglenids as a whole, as well as for a better understanding of the relationships with their closest euglenozoan relatives, the Kinetoplastida and the Diplonemida. I generated DNA sequences of heat shock protein 90 and small subunit (SSU) rRNA genes from several different species of phagotrophic euglenids in order to evaluate some of the deepest branches in the phylogeny of euglenozoans, especially the phylogenetic position of Petalomonas cantuscygni. This species has a set of morphological features that are intermediate between kinetoplastids and euglenids (e.g., pellicle strips and kinetoplast-like mitochondrial inclusions). I also characterized the ultrastructure, feeding behaviour, and phylogenetic position of Heteronema scaphurum, a phagotrophic euglenid that feeds on green algal prey and is equipped with a distinctive “cytoproct” or cell anus. My explorations in low oxygen marine sediments led me to discover and characterize a novel lineage of euglenozoans, the “Symbiontida”. Members of this group formed intimate symbiotic relationships with at least two distinct types of epibiotic bacteria: rod-shaped epsilon-proteobacteria and spherical-shaped verrucomicrobia. I was able to show, using electron microscopy, that the verrucomicrobial symbionts were capable of evasive sporulation using a conspicuous extrusive apparatus that consisted of a thread tightly wound around a central core of DNA. The highly similar episymbionts reported previously on a group of ciliates led to questions about host transfer and the convergent evolution of extrusive organelles across the tree of eukaryotes.

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Comparative Morphology and Molecular Evolution of Marine Interstitial Cercozoans (2009)

No abstract available.

Morphological evolution and development of the euglenid cytoskeleton (2009)

In an effort to better understand character evolution in the cytoskeleton (pellicle) of euglenid protists, I used comparative and descriptive methods to investigate the morphological diversity and development of pellicle surface patterns formed by differences in strip length at the anterior and posterior ends of the cell (strip reduction). By observing dividing Euglena gracilis cells with scanning electron microscopy (SEM) and integrating these data with previous evolutionary and developmental research, I showed that these patterns result from the semiconservative duplication and subsequent intermittent growth of pellicle strips during cytoskeletal replication and cytokinesis. Furthermore, simple changes in the developmental timing of this process (heterochrony) resulted in the diversity of posterior strip reduction patterns observed in phototrophic euglenids. This model was then used to interpret the results of two studies describing pellicle surface patterns in other photosynthetic taxa. The first was a morphological description of the complex linear pattern of posterior reduction in the benthic marine phototroph, Euglena obtusa. The second was an investigation of the evolution of bilaterally symmetrical, “clustered” strip reduction patterns in the rigid genus Phacus, examined in the context of maximum likelihood (ML) and Bayesian phylogenetic analyses of combined nuclear small subunit and partial large subunit ribosomal genes (SSU rDNA and LSU rDNA, respectively). These studies, taken together, show that strip length and other pellicle characters (such as pore placement) are strongly influenced by age and perhaps other developmental factors (such as parental strip identity and cell polarity), but the underlying genetics and molecular biology of these factors are completely unknown. Finally, SEM was used for the first time to describe prearticular strip projections, a pellicle character that has been extensively studied using transmission electron microscopy (TEM). The novel character state revealed by this study shows that the diversity of this pellicle character is still poorly understood. The structural complexity of the euglenid pellicle and the developmental and evolutionary processes that resulted in its astonishing diversity could make it an ideal model system for studying cytoskeletal evolution and development once a robust genetic research framework is constructed.

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Master's Student Supervision (2010 - 2018)
Species discovery, evolution and kleptoplasty in marine meiofaunal flatworms (2018)

Rhabdocoel flatworms are abundant members of marine meiofaunal communities worldwide,contributing to a reservoir of biodiversity that thrives between grains of sand. However, theyare relatively understudied due to bias in meiofaunal sampling techniques and a lack oftaxonomic expertise. Here, five species of neodalyellid rhabdocoels were discovered fromintertidal habitats in British Columbia and characterised with molecular and morphologicaldata: Baicalellia solaris n. sp., Baicalellia daftpunka n. sp., Tamanawas kalipis n. sp.,Pogaina paranygulgus and Baicalellia pusillus. A molecular phylogenetic analysis usingmaximum likelihood and Bayesian inference on concatenated 18S and 28S rDNA sequencesprovided a framework for revising neodalyellid systematics and for inferring characterevolution within the group. Kleptoplasty, the phenomenon by which one organism stealsplastids from another, was discovered in the “solar panel worms” B. solaris and P.paranygulgus, representing just the second case in metazoans; kleptoplasty has only beendescribed previously in sacoglossan sea slugs. Using a combination of light and electronmicroscopy, I demonstrated that plastids were intracellularly sequestered in the parenchymaltissue. DNA barcoding of partial rbcL sequences demonstrated that the plastids were stolenfrom raphid pennate diatoms, which was consistent with plastid ultrastucture. Measurementsof oxygen consumption demonstrated that kleptoplasts remain functional for at least ten daysafter sequestration in B. solaris cells. Photosynthetic activity was of a similar magnitude to adense chlorophyte culture, indicating that photosynthetically-fixed carbon enhanced survivalin light-treated compared with dark-treated flatworms. Kleptoplasts ultimately lose functionand are digested; therefore, heterotrophy is required to replenish healthy populations ofkleptoplasts within the host tissue. The kleptoplasts might serve as a food store, providingsustenance when seasonal diatom blooms collapse. It cannot be determined whetherkleptoplasty arose once in the common ancestor of Pogaina and Baicalellia or has evolvedtwice convergently.

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Description of two new species of marine gregarine parasites (Apicomplexa) from the intestines of Lumbrineris inflata (Annelida) (2017)

Apicomplexans are diverse single-celled eukaryotes that parasitize animals. The most notorious members include those of particular human interest such as the causative agents of malaria, toxoplasmosis, and cryptosporidiosis. While a subset of apicomplexans has been intensively studied from a medical or veterinary perspective, the diversity of remaining groups is underrepresented in existing literature. This lack of data has left the deep relationships among apicomplexan taxa enigmatic and in turn has hindered the revelation of some major evolutionary processes that sparked the apicomplexan radiation. The dearth of understanding surrounding apicomplexan systematics can be addressed in part through the discovery of novel species and the identification of how morphological and molecular characters are distributed across the apicomplexan phylogeny. Some lineages of marine gregarines have retained plesiomorphic characters that offer unique insight into the earliest stages of apicomplexan evolution. The current thesis describes and establishes two novel marine gregarine species isolated from a polychaete hosts (Lumbrineris inflata). Species delimitation and description was based on morphological data acquired using light and electron microscopy and a molecular phylogenetic analysis of 18S small subunit (SSU) rDNA sequences. Paralecudina anankea n. sp. possessed an elongated body, an oval nucleus, and gliding motility. The sister relationship of P. anankea n. sp. with P. polymorpha was robustly supported by molecular phylogenetic analysis (100 MLB, 1.00 BPP) and the SSU rDNA sequences between the two were 12% divergent. In contrast, L. caspera n. sp. was morphologically dissimilar to its closest relative L. longissima and possessed an acorn-shaped body, a distinct mucron, and gliding motility. Molecular phylogenetic analysis recovered L. caspera n. sp. as a sister species to L. longissima with strong support (100 MLB, 1.00 BPP) and their SSU rDNA sequences which were 8% divergent. The generation of additional morphological and molecular traits in gregarines will improve the phylogenetic resolution of the apicomplexan backbone and improve inferences about the evolutionary transition from photosynthetic ancestors to obligate parasites.

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Molecular contributions to species descriptions of dicyemid mesozoans (2013)

Dicyemids are enigmatic parasites found only within the excretory systems of benthic cephalopods. Over the past century, dicyemids have been considered to be either complex protozoa, “mesozoa” that are ambiguously intermediate between protozoa and metazoa, or reduced metazoans. The phylogenetic position and overall diversity of dicyemids is poorly understood. Current species identification criteria are unconvincing because they are based solely on morphological traits. I set out to test current morphological species concepts with DNA barcodes from dicyemids collected from Pacific Northwest cephalopods. Variation within sequences of the small subunit (18S) rRNA gene was explored because this marker (1) is known to be fast-evolving in parasitic eukaryotes, (2) is one of the few molecular markers to have been previously sequenced in some dicyemids, and (3) has been used successfully as a barcode in other groups of parasites. Three host species of cephalopods were collected in this study, each hosting multiple historical morphospecies of dicyemid parasites. Thirty-four individual dicyemids encompassing eight morphospecies were isolated and their 18S rDNA sequenced. Molecular phylogenetic analyses of these data were incongruent with current morphology-based species concepts. The 18S rDNA sequences suggest that each host species of cephalopod harbors only one species of dicyemid with a great deal of morphological variation. However, the 18S rDNA sequences should eventually be tested with other rapidly evolving molecular markers. Attempts were made to sequence the mitochondrial cytochrome oxidase I (COI) gene, the mitochondrial 16S rRNA gene, and both Internal Transcribed Spacers (ITS) of the nuclear rRNA operon. With so little of the dicyemid genome known, I was unable to establish reliable primer pairs for these genes within the time constraints of my MSc thesis. Nonetheless, this study has shown that DNA barcoding is a powerful tool for the delimitation of dicyemid species. Understanding the diversity of parasite species is particularly problematic because they tend to be devoid of consistent (informative) morphological traits while simultaneously rich in morphological variation associated with developmental stages and environmental conditions. The addition of DNA barcodes to dicyemid diversity will simplify and improve species boundaries in a lineage that is difficult to define in every aspect.

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Contributions to the molecular phylogeny, phylogeography, and taxonomy of scyphozoan jellyfish (2012)

Scyphozoan jellyfish are a major group of large, bloom-forming marine animals that can disrupt ecological stability and interfere with marine-oriented industries. The widespread geographical distributions and high degrees of morphological plasticity within many species make understanding the overall diversity of scyphozoans difficult. Molecular phylogenetic approaches have the potential to offer powerful insights into many aspects of scyphozoan biology, such as species identification, evolutionary history, and phylogeography that will improve our ability to monitor and manage the roles these animals play in marine ecosystems. We established datasets of 16S rDNA and cytochrome c oxidase subunit I (COI) sequences of several different species of scyphozoans in order to better understand phylogenetic, phylogeographical, and taxonomic patterns within the group. Phylogenetic analysis of 16S rDNA sequences resolved closely related taxa but was too variable to resolve deeper relationships with robust statistical support. Combining this marker with a more conserved dataset of nuclear 18S rDNA sequences resulted in a phylogenetic tree with clades that had higher statistical support than in trees inferred from each marker alone. 16S rDNA sequences also showed phylogeographical patterns in Cyanea, distinguishing clearly between a Northeastern Pacific (NEP) clade and a Northwestern Atlantic clade (NWA) (9.71 - 9.93% mean genetic difference MGD), as well as two Atlantic subclades (NWA1, NWA2) (1.79% MGD). Distances within clades ranged from 0.05 - 0.2%. Therefore, 16S rDNA sequences were able to delimit different (putative) species that reflected distinct geographical distributions. In addition, comparative analyses of morphological features and COI sequences from Northeast Pacific isolates of Cyanea demonstrated that C. ferrugenia is a valid lion’s mane species found in the Northeast Pacific Ocean.

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