Person: Laumer, Christopher
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Laumer
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Christopher
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Laumer, Christopher
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Publication Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation(eLife Sciences Publications, Ltd, 2015) Laumer, Christopher; Hejnol, Andreas; Giribet, GonzaloFlatworms number among the most diverse invertebrate phyla and represent the most biomedically significant branch of the major bilaterian clade Spiralia, but to date, deep evolutionary relationships within this group have been studied using only a single locus (the rRNA operon), leaving the origins of many key clades unclear. In this study, using a survey of genomes and transcriptomes representing all free-living flatworm orders, we provide resolution of platyhelminth interrelationships based on hundreds of nuclear protein-coding genes, exploring phylogenetic signal through concatenation as well as recently developed consensus approaches. These analyses robustly support a modern hypothesis of flatworm phylogeny, one which emphasizes the primacy of the often-overlooked ‘microturbellarian’ groups in understanding the major evolutionary transitions within Platyhelminthes: perhaps most notably, we propose a novel scenario for the interrelationships between free-living and vertebrate-parasitic flatworms, providing new opportunities to shed light on the origins and biological consequences of parasitism in these iconic invertebrates. DOI: http://dx.doi.org/10.7554/eLife.05503.001Publication Inclusive Taxon Sampling Suggests a Single, Stepwise Origin of Ectolecithality in Platyhelminthes(Wiley-Blackwell, 2014) Laumer, Christopher; Giribet, GonzaloEctolecithality is a form of oogenesis unique within Metazoa but common in Platyhelminthes, in which almost yolkless oocytes and tightly associated yolk cells are deposited together in egg capsules. Despite profound impacts on the embryogenesis and morphology of its beneficiaries, the origins of this developmental phenomenon remain obscure. Traditionally, all ectolecithal flatworms were grouped in a clade called Neoophora. However, there are also morphological arguments for multiple origins of ectolecithality and, to date, Neoophora has seen little support from molecular phylogenetic research, largely as a result of gaps in taxon sampling. Accordingly, we present a molecular phylogeny focused on resolving the deepest divergences among the free-living Platyhelminthes. Species were chosen to completely span the diversity of all major endo- and ectolecithal clades, including several aberrant species of uncertain systematic affinity and, additionally, a thorough sampling of the ‘lecithoepitheliate’ higher taxa Prorhynchida and Gnosonesimida, respectively, under- and unrepresented in phylogenies to date. Our analyses validate the monophyly of all classical higher platyhelminth taxa, and also resolve a clade possessing distinct yolk-cell and oocyte generating organs (which we name Euneoophora new taxon). Furthermore, implied-weights parsimony and Bayesian mixture model analyses suggest common ancestry of this clade with the lecithoepitheliates, implying that these taxa may retain a primitive form of ectolecithality. This topology thus corroborates the classical hypothesis of homology between yolk cells and oocytes in all Neoophora, and should serve to guide future evolutionary research on this unique developmental innovation in Platyhelminthes.Publication New Insights into the Phylogeny, Systematics and DNA Barcoding of Nemertea(CSIRO Publishing, 2014) Kvist, Sebastian; Laumer, Christopher; Junoy, Juan; Giribet, GonzaloAlthough some clades of ribbon worms (phylum Nemertea) are consistently recovered with high support in molecular phylogenies, the placement and inter-relationships of some taxa have proven problematic. Herein, we performed molecular phylogenetic analyses aimed at resolving these recalcitrant splits, using six loci (nuclear 18S rRNA, 28S rRNA, histones H3 and H4, and mitochondrial 16S rRNA and COI) for 133 terminals, with particular emphasis on the problematic families Hubrechtidae and Plectonemertidae. Three different datasets were used for phylogenetic analyses and both maximum likelihood and maximum parsimony methodologies were applied. All but one of the resulting tree topologies agree on the paraphyly of the class Palaeonemertea, whereas Heteronemertea, Hoplonemertea, Polystilifera, Monostilifera and Hubrechtidae are always recovered as reciprocally monophyletic. Hubrechtidae is sister group to Heteronemertea (the Pilidiophora hypothesis) only when length variable regions of 18S rRNA and 28S rRNA are excluded. Moreover, the terrestrial and freshwater family Plectonemertidae is recovered with high support and the implications of this finding are further discussed. Finally, we evaluate the utility of DNA barcoding for specimen identification within Nemertea using an extended dataset containing 394 COI sequences. Results suggest that DNA barcoding may work for Nemertea, insofar as a distinct barcoding gap (the gap between the maximum intraspecific variation and the minimum interspecific divergence) may exist, but its recognition is regularly hampered by low accuracy in species level identifications.Publication Isolated branches in the phylogeny of Platyhelminthes(2015-03-06) Laumer, Christopher; Giribet, Gonzalo; Edwards, Scott V.; Extavour, Cassandra G.; Hochberg, RickThis dissertation examines the early phylogenetic divergences of the phylum Platyhelminthes using molecular sequence data, with an emphasis on the placement and evolutionary significance of several enigmatic and largely overlooked lineages. Firstly, I assess platyhelminth interrelationships using a representational sampling of all free-living orders for the “standard” 18S and 28S rRNA loci (plus two mtDNA markers). These analyses place numerous problematic taxa, most notably Gnosonesimida, which is recovered in a position consistent with the classical hypothesis in which this order retains a primitive form of ectolecithality. I also investigate the status of the crustacean-parasitic genus Genostoma, classified presently within Fecampiida, which has however been proposed on the basis of ultrastructural data to lie outside this order. These efforts robustly position Genostoma as the sister-taxon to the free-living order Prolecithophora, suggesting the recognition of a new higher taxon to accommodate this morphologically distinct, but poorly diverse lineage. To overcome the inherent limits of rRNA phylogenetics, I used massively parallel sequencing to survey transcriptomes from representatives of all “turbellarian” orders. From concatenation and consensus analyses of 512 orthologs, a robust signal of platyhelminth phylogeny emerges, congruent with previous results but also presenting several unanticipated relationships. Most notable among these, the monospecific order Bothrioplanida is recovered as the sister-group of Neodermata, the major vertebrate-parasitic clade within Platyhelminthes. These analyses prompt consideration of novel hypotheses on the origins and consequences of parasitism within Platyhelminthes, and motivate many previously unexplored comparisons among free-living taxa. The position of Platyhelminthes within Spiralia, and the related question of whether the phylum is “primitive” in morphology, remains controversial. I therefore also used transcriptomic data to resolve the phylogeny of Spiralia, with emphasis on the status of the “platyzoan” phyla, and on positioning several problematic interstitial lineages. These data robustly position Lobatocerebrum and Diurodrilus as members of Annelida. I also recover strong support for the non-monophyly of the platyzoan phyla, with Gnathifera as the earliest-splitting branch and a clade of Platyhelminthes and Gastrotricha as the nearest relative of Trochozoa. This phylogeny hence simultaneously highlights the importance of “reductive” processes in the evolution of interstitial organisms, as well as the possibility of the primitive nature of at least some of the “simple” features that have classically inspired zoological interest in Platyhelminthes. Finally, I present a focused inquiry on the internal phylogeny of one “isolated” flatworm clade, the continental order Prorhynchida. The recovered topology is broadly congruent with traditional classification, with most prorhynchid species falling into two genera. Remarkably, however, two rare taxa that share morphologically similar copulatory apparatus are recovered as unrelated basal branches, indicating the probable plesiomorphic nature of this morphology. Also, a little-known groundwater species, Geocentrophora boui, is supported as the sister taxon of the self-fertilizing genus Xenoprorhynchus, illuminating the functional specialization of the “copulatory” apparatus as a venom delivery system in this lineage. Field collections from this study uncovered over 31 new species, many of these unexpectedly terrestrial, more than doubling the known diversity of the order, and highlighting the need for continued systematic research on these remarkable but understudied animals.