Population genomics, systematics, and phylogenomics of the tapeworm order Trypanorhyncha

Abstract

The order Trypanorhyncha is a ubiquitous and speciose group of commercially relevant marine tapeworms. As adults, trypanorhynchs inhabit the guts of sharks and rays (i.e., elasmobranchs). They sport attachment organs with highly characteristic hooked tentacles and are further unique among the nine orders of shark and ray-hosted tapeworms in demonstrating variable degrees of specificity for their elasmobranch hosts. Adult trypanorhynchs from elasmobranchs, and their larval counterparts from bony fishes, molluscs, and crustaceans, have been collected for centuries. Despite this attention, however, the order remains notorious as “the most chaotic and confused of tapeworm groups” (Wardle & McLeod, 1952; The Zoology of Tapeworms pg. 287). Drivers of chaos include the misinterpretation of distinguishing morphological features, species descriptions based only on larval specimens, and an evolutionary hypothesis for the order that is at odds with a classification based on morphology. This dissertation leverages a variety of data types and methodological approaches to present a refined understanding of diversity, morphology, population genomics, and evolutionary history for the trypanorhynch tapeworms. In Chapter 1, the trypanobatoid family Rhinoptericolidae Carvajal & Campbell, 1975 is revised based on global collections and an integrative taxonomic approach. Membership in the family is increased through the description of new species and the transfer of previously described species. The importance of scanning electron microscopy for accurate interpretation of tentacular armature is demonstrated, and the first comprehensive evaluation of intraspecific and intrageneric divergence in the tapeworm barcoding gene for trypanorhynch tapeworms is presented. Finally, a phylogenetic analysis based on sequence data is the first to recover a monophyletic Rhinoptericolidae, and a novel schematic to aid comprehension of line drawings and scanning electron micrographs of the tentacular armature is introduced. Chapter 2 represents the first investigation of population genomics for trypanorhynch tapeworms, and for elasmobranch tapeworms more broadly. A restriction-site associated DNA (RAD) sequencing approach is used to characterize population structure and genetic diversity for two species of trypanorhynchs that demonstrate relaxed host specificity. These are Rhinoptericola megacantha Carvajal & Campbell, 1975 (suborder Trypanobatoida) and Callitetrarhynchus gracilis (Rudolphi, 1819) Pintner, 1931 (suborder Trypanoselachoida). For each species, worms were sampled from multiple species of their known elasmobranch hosts from across their known geographic distributions. Sampling also emphasized sequencing worms from multiple conspecific host individuals within and between geographic regions, and sequencing multiple worms from the same host individual, wherever possible. For R. megacantha, population structure coincides with geographic region rather than definitive host species. For C. gracilis, limited population structure is found. Both species exhibit high levels of homozygosity and elevated FIS values. Conspecific tapeworms collected from the same host individual are as, or more, genetically divergent from one another as from conspecifics collected from different host individuals. Additionally, examination of material from tens of carcharhiniform sharks suggests that adults of C. gracilis may be restricted to parasitizing species in the family Carcharhinidae Jordan & Evermann, 1896. Chapter 3 presents the first phylogenomic hypothesis for the order Trypanorhyncha. Multispecies coalescent and multigene concatenation-based tree building approaches are employed to analyze data for hundreds of orthologous loci from more than 200 trypanorhynchs representing all major lineages within the order. These analyses expand on prior sequencing efforts for the order, both in terms of the number of loci sequenced and the proportion of trypanorhynch diversity represented. Support for the two existing suborders is recovered, but need for major changes to inclusion in, and organization of, superfamilies, families, and genera is evident—particularly for the suborder Trypanobatoida. Support is recovered for multiple independent losses of the rhyncheal system, and new taxa hosted by species of elasmobranchs previously unexamined for trypanorhynch tapeworms are identified as targets for future descriptive work.