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Award Abstract # 1921404
Collaborative Research: Cestode phylogeny and genomics

NSF Org: DEB
Division Of Environmental Biology
Recipient: UNIVERSITY OF CONNECTICUT
Initial Amendment Date: August 19, 2019
Latest Amendment Date: June 18, 2021
Award Number: 1921404
Award Instrument: Continuing Grant
Program Manager: Christopher Balakrishnan
cbalakri@nsf.gov
 (703)292-2331
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: September 1, 2019
End Date: August 31, 2024 (Estimated)
Total Intended Award Amount: $1,209,967.00
Total Awarded Amount to Date: $1,217,743.00
Funds Obligated to Date: FY 2019 = $419,274.00
FY 2020 = $347,227.00

FY 2021 = $451,242.00
History of Investigator:
  • Janine Caira (Principal Investigator)
    janine.caira@uconn.edu
  • Elizabeth Jockusch (Co-Principal Investigator)
  • Jill Wegrzyn (Co-Principal Investigator)
Recipient Sponsored Research Office: University of Connecticut
438 WHITNEY RD EXTENSION UNIT 1133
STORRS
CT  US  06269-9018
(860)486-3622
Sponsor Congressional District: 02
Primary Place of Performance: University of Connecticut
75 N. Eagleville Rd. Unit 3043
Storrs
CT  US  06269-3043
Primary Place of Performance
Congressional District:
02
Unique Entity Identifier (UEI): WNTPS995QBM7
Parent UEI:
NSF Program(s): Systematics & Biodiversity Sci
Primary Program Source: 01001920DB NSF RESEARCH & RELATED ACTIVIT
01002021DB NSF RESEARCH & RELATED ACTIVIT

01002122DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 102Z, 9251
Program Element Code(s): 737400
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Tapeworms are parasites that include numerous species of medial and veterinary importance in mammals as well as thousands of species that parasitize essentially all other groups of vertebrate animals. Yet, we know little about the evolution of the major groups of tapeworms. Not only does this hamper our ability to treat tapeworm infections of medical and veterinary importance, but it also limits the use of tapeworms as model parasite systems to help expand our understanding of food web connections and ecosystem health, and to help inform fisheries management practices. This project aims to generate the molecular and morphological data required to substantially expand our understanding of the evolution of tapeworms. In doing so, it will transform tapeworms and their vertebrate hosts into one of the best known host/parasite systems globally, allowing this system to reach its full potential. The training provided to undergraduate, graduate and postdoctoral researchers will equip them with transferable STEM skills. Furthermore, information about tapeworms will be made publicly available on-line to diverse audiences of all ages by creating a key to the major tapeworm groups, developing an e-book version of a children's book on tapeworms, and building upon an existing global cestode database.

A recent global survey has identified tapeworm lineages hosted by sharks and rays as central to the diversification of the Cestoda. This class currently comprises 19 orders. Preliminary phylogenetic work suggests that the current ordinal classification of the class substantially underestimates lineage diversity, especially within the groups of elasmobranch-hosted cestodes. The proposed work aims to provide a robust phylogeny of the class based on targeted gene capture of 738 loci for 960 species of tapeworms. Cestode higher-level classification will be revised to reflect monophyletic groups, informed by new morphological and molecular data. The generation of complete genomes for 20 species spanning the approximately 200-million year gap between the cestodes of medical and veterinary importance for which such data are currently available will provide insight into patterns of taxon-specific gene family evolution across cestodes. Genomic analyses have been designed to take advantage of the multiple independent transitions between marine and non-marine habitats, elasmobranch and non-elasmobranch definitive hosts, and invertebrate and vertebrate final intermediate hosts that have occurred over evolutionary time to identify signatures of parallel evolution. Such signatures are anticipated to provide valuable insight into environmental factors that may have played a role in the evolution of parasite systems with complex life cycles.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 23)
BUENO, VERONICA M. and CAIRA, JANINE N. "Phylogenetic relationships, host associations, and three new species of a poorly known group of tetraphyllidean tapeworms from elasmobranchs" Zootaxa , v.5254 , 2023 https://doi.org/10.11646/zootaxa.5254.1.2 Citation Details
Bueno, V M and Trevisan, B and Caira, J N "Phylogeny of the cestode family Escherbothriidae (Cestoda: Rhinebothriidea) reveals unexpected patterns of association with skate hosts" Invertebrate Systematics , v.38 , 2024 https://doi.org/10.1071/is23056 Citation Details
Caira, Janine N and Bueno, Veronica and Jensen, Kirsten "Emerging global novelty in phyllobothriidean tapeworms (Cestoda: Phyllobothriidea) from sharks and skates (Elasmobranchii)" Zoological Journal of the Linnean Society , 2021 https://doi.org/10.1093/zoolinnean/zlaa185 Citation Details
Caira, Janine N. and Jensen, K. "Diversity and phylogenetic relationships of 'tetraphyllidean' Clade 3 (Cestoda) based on new material from orectolobiform sharks in Australia and Taiwan" Folia Parasitologica , v.69 , 2022 https://doi.org/10.14411/fp.2022.010 Citation Details
Caira, Janine N. and Jensen, Kirsten "Electron microscopy reveals novel external specialized organs housing bacteria in eagle ray tapeworms" PLOS ONE , v.16 , 2021 https://doi.org/10.1371/journal.pone.0244586 Citation Details
CAIRA, JANINE N. and JENSEN, KIRSTEN "

Two new species of Caulobothrium (Cestoda: Tetraphyllidea) from the duckbill eagle ray, Aetomylaeus bovinus (Myliobatiformes: Myliobatidae), off Senegal with new insights on morphological features of the genus Zootaxa , v.4903 , 2021 https://doi.org/10.11646/zootaxa.4903.1.8 Citation Details

Caira, Janine N. and Jensen, Kirsten and Pickering, Maria and Ruhnke, Timothy R. and Gallagher, Kaitlin A. "Intrigue surrounding the life-cycles of species of Clistobothrium (Cestoda: Phyllobothriidea) parasitising large pelagic sharks" International Journal for Parasitology , v.50 , 2020 https://doi.org/10.1016/j.ijpara.2020.08.002 Citation Details
Caira, Janine N. and Otto, Kyle and Fernando, Daniel and Jensen, Kirsten "Three new species of 'tetraphyllidean' cestodes from an undescribed bamboo shark (Orectolobiformes: Hemiscylliidae) in Sri Lanka" Folia Parasitologica , v.68 , 2021 https://doi.org/10.14411/fp.2021.004 Citation Details
Caira, J.N. and Jensen, K. and Hayes, C. and Ruhnke, T.R. "Insights from new cestodes of the crocodile shark, Pseudocarcharias kamoharai (Lamniformes: Pseudocarchariidae), prompt expansion of Scyphyophyllidum and formal synonymization of seven phyllobothriidean genera at last!" Journal of Helminthology , v.94 , 2020 10.1017/S0022149X20000036 Citation Details
Caira, J. N. and Pickering, M. and Jensen, K. "Expanding known global biodiversity of Yamaguticestus (Cestoda: Phyllobothriidea) parasitizing catsharks (Pentanchidae and Scyliorhinidae)" Systematics and Biodiversity , v.19 , 2021 https://doi.org/10.1080/14772000.2021.1946617 Citation Details
Gallagher, K. A. and Caira, J. N. "A New Species of Acanthobothrium (Cestoda: Onchoproteocephalidea) from the Smalleye Pygmy Shark, Squaliolus aliae (Chondrichthyes: Squaliformes: Dalatiidae), from Taiwan" Journal of Parasitology , v.106 , 2020 https://doi.org/10.1645/20-15 Citation Details
(Showing: 1 - 10 of 23)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Ours was the first study to employ a targeted gene capture approach for tapeworms. We have developed ~400 orthogroups (~1,000+ exons) with varying degrees of phylogenetic signal and thus of potential application for phylogenetic work in other groups of flatworms beyond tapeworms (e.g., digeneans, monogeneans). The project resulted in the publication of 1 new family, 7 new genera, and descriptions of 73 new species. Our phylogeny represents the most comprehensive and robust phylogeny of tapeworms available. It reveals that the tapeworms of elasmobranchs are key to the evolution of all groups of acetabulate tapeworms. One of the most interesting outcomes of our work is that it has provided strong evidence that the Cyclophyllidea—the order that includes not only the majority of species that parasitize birds, mammals, amphibians, and herptiles, but almost all of the species of tapeworms that parasitize terrestrial vertebrates—had its origins in the tapeworms that parasitize elasmobranchs. While the evidence is not definitive, it suggests that origin involved a group of batoids. The phylogeny revealed hundreds of the species across the topology that are new to science. The fact that the molecular work required to confirm that novelty has already been conducted paves the way for the descriptive work required to formally describe these species. The phylogeny also serves as a framework for future work on the evolution of tapeworms. A species level tree for tapeworms serves as a resource for future work investigating the evolution of morphological traits, adaptations to attachment to host mucosa, diversification across lineages, and, given we have also generated a species-level tree for the hosts, cophylogenetic signal between the tapeworms and their elasmobranch hosts. The revised classification changes the landscape of our understanding of higher-level diversity in the tapeworms of elasmobranchs. We have resolved the rampant polyphyly of the suite of taxa known as the “tetraphyllidean relicts”. As a result of the new classification all orders of tapeworms are now monophyletic and can be investigated as unified evolutionary units. It also provides a definitive answer to the question of whether hooks that have been shown to be composed of different proteins are homologous—the answer is a resounding NO! The tapeworms that possess hooks represents 6 distinct mutually monophyletic orders, none of which are each other’s closest relatives. We are the first to assemble genomes for any of the orders that parasitize elasmobranchs and bonyfish. Prior to our work, genome data were limited to a handful of species of medical importance in the cestode orders Cyclophyllidea and Diphyllobothriidea. By assembling genomes for taxa across the phylogenetic tree of eucestodes we have provided important context. We engaged 2 postdoctoral fellows, 2 technicians, 7 graduate students, 13 undergraduate students and 1 post-bac student. We collectively presented a total of 36 talks at regional, national, and international meetings. The project resulted in a total of 23 publications. We completed the development of the web application for the visual, multi-entry, interactive online key to the identification of elasmobranch tapeworm genera (https://tapeworms-unlocked.info). Finally, we produced an interactive online version of our children’s book “Meet the Suckers” which can also be accessed via the tapeworm key site (https://book.tapeworms-unlocked.info/).


Last Modified: 02/28/2025
Modified by: Janine N Caira

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