Phylogenetics & Systematics
LEFT: A hypothesis of cestode evolution from the 1950s monograph of Emer Prof Louis Euzet superimposed atop the molecular sequence data that have enlightened the way we infer evolution today | illustration PD Olson
LEFT: A hypothesis of cestode evolution from the 1950s monograph of Emer Prof Louis Euzet superimposed atop the molecular sequence data that have enlightened the way we infer evolution today | illustration PD Olson
Examples of unsegmented tapeworms: (left) a caryophyllidean, (center) a spathebothriidean, and (right) an example of secondary loss of segmentation (Olson et al., 2001) in the pseudophyllidean, Anantrum tortum. The retention of multiple reproductive sets (ie. proglottides) in the loss of external segmentation as seen in A. tortum (and in all spathebothriidean tapeworms) demonstrates that 'segmentation' involves two independent processes that may be de-coupled by evolution.
An lsrDNA-based hypothesis of tapeworm evolution (Olson et al., 2001) indicating independent evolutionary acquisitions of 'proglottization' (serial development of proglottides) and 'strobilation' (the somatic compartmentalization of the proglottides).
Phylogenetics and systematics of the parasitic flatworms
One arm of our research addresses the biodiversity and phylogeny of parasitic flatworms (flukes, tapeworms and 'monogeneans'), using this information to construct natural classifications and to infer ancestral conditions.
RELATED PUBLICATIONS:
Hrčkova G, M Mitterpáková, A O'Connor, V Šnábel and PD Olson. 2011. Molecular and morphological circumscription of Mesocestoides tapeworms from red foxes (Vulpes vulpes) in central Europe. Parasitology 138:638-647
Olson PD, LG Poddubnaya, DTJ Littlewood and T Scholz. 2008. On the position of Archigetes and its bearing on the early evolution of the tapeworms. Journal of Parasitology 94:898-904
Olson PD and VV Tkach. 2005. Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 60:165-243
Olson PD, TH Cribb, VV Tkach, RA Bray and DTJ Littlewood. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33:733-755
Cribb THC, RA Bray, PD Olson and DTJ Littlewood. 2003. Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54:197-254
Olson PD and DTJ Littlewood. 2002. Invited Review: Phylogenetics of the Monogenea—evidence from a medley of molecules. International Journal for Parasitology 32:233-244
Olson PD, DTJ Littlewood, RA Bray and J Mariaux. 2001. Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 18:443-467
Littlewood DTJ and PD Olson. 2001. Small subunit rDNA and the phylum Platyhelminthes: signal, noise, conflict and compromise. In Interrelationships of the Platyhelminthes (DTJ Littlewood and RA Bray, Eds.), pp. 262-278
Mariaux J and PD Olson. 2001. Cestode phylogenetics in the molecular era. In Interrelationships of the Platyhelminthes (DTJ Littlewood and RA Bray, Eds.), pp. 127-134. Taylor & Francis, London
Olson PD and JN Caira. 1999. Evolution of the major lineages of tapeworms (Platyhelminthes: Cestoidea) inferred from 18S ribosomal DNA and elongation factor-1α. Journal of Parasitology 85:1134-1159
One arm of our research addresses the biodiversity and phylogeny of parasitic flatworms (flukes, tapeworms and 'monogeneans'), using this information to construct natural classifications and to infer ancestral conditions.
RELATED PUBLICATIONS:
Hrčkova G, M Mitterpáková, A O'Connor, V Šnábel and PD Olson. 2011. Molecular and morphological circumscription of Mesocestoides tapeworms from red foxes (Vulpes vulpes) in central Europe. Parasitology 138:638-647
Olson PD, LG Poddubnaya, DTJ Littlewood and T Scholz. 2008. On the position of Archigetes and its bearing on the early evolution of the tapeworms. Journal of Parasitology 94:898-904
Olson PD and VV Tkach. 2005. Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 60:165-243
Olson PD, TH Cribb, VV Tkach, RA Bray and DTJ Littlewood. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33:733-755
Cribb THC, RA Bray, PD Olson and DTJ Littlewood. 2003. Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54:197-254
Olson PD and DTJ Littlewood. 2002. Invited Review: Phylogenetics of the Monogenea—evidence from a medley of molecules. International Journal for Parasitology 32:233-244
Olson PD, DTJ Littlewood, RA Bray and J Mariaux. 2001. Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 18:443-467
Littlewood DTJ and PD Olson. 2001. Small subunit rDNA and the phylum Platyhelminthes: signal, noise, conflict and compromise. In Interrelationships of the Platyhelminthes (DTJ Littlewood and RA Bray, Eds.), pp. 262-278
Mariaux J and PD Olson. 2001. Cestode phylogenetics in the molecular era. In Interrelationships of the Platyhelminthes (DTJ Littlewood and RA Bray, Eds.), pp. 127-134. Taylor & Francis, London
Olson PD and JN Caira. 1999. Evolution of the major lineages of tapeworms (Platyhelminthes: Cestoidea) inferred from 18S ribosomal DNA and elongation factor-1α. Journal of Parasitology 85:1134-1159
image RM Overstreet
Flatworm parasites of sharks and rays
Evolutionarily, the parasitic flatworms were first and foremost parasites of fishes, parasitizing both bony and cartilaginous groups for probably as long as these great lineages have existed. Contemporary sharks and rays are host to an extraordinary parasite fauna, which is especially diverse in cestodes (5 of ~14 orders of cestodes are found exclusively in elasmobranchs).
My interest in these parasites began as a PhD student working with Janine Caira at the University of Connecticut. Janine's group have discovered, documented and studied these parasites for over 20 years and continue to travel the world in pursuit of new fauna.
Evolution of the Trypanorhyncha
Our most recent work in molecular phylogenetics represents 10-years of sampling trypanorhynch diversity around the globe, mostly through the help of collaborators, including Janine, Ian Beveridge, Kirsten Jensen and Robin Overstreet (see Collaborators). These specimens have been characterized both genetically and morphologically and deposited in well-curator museums. The study has revealed a great deal about the interrelationships of the various trypanorhynch lineages, and has shown that there is tremendous plasticity in the form of their tentacular armature, their primary taxonomic features.
Looking at the pattern of their evolution more broadly, we see that the group comprises two main lineages, and by examining the distribution of host associations within these lineages we find a distinct lineage of shark parasites and a distinct lineage of ray parasites. The most parsimonious explanation for this distribution is that sharks and rays themselves followed separate evolutionary paths which resulted in their parasites evolving independently. This overturns the notion that rays are derived from sharks (known as the 'Hypnosqualea' hypothesis; Shirai) and supports recent molecular estimates of elasmobranch evolution.
RELATED PUBLICATIONS:
PD Olson, JN Caira, K Jensen, H Palm, R Overstreet and I Beveridge. 2010. Evolution of the trypanorhynch tapeworms: parasite phylogeny supports independent lineages of sharks and rays. International Journal for Parasitology 40:223-242
Palm HW, A Waeschenbach, PD Olson and DTJ Littlewood. 2009. Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 52:351-367
Aznar FJ, C Agusti, DTJ Littlewood, JA Raga and PD Olson. 2007. Insight into the role of cetaceans in the life cycle or tetraphyllideans (Platyhelminthes: Cestoda). International Journal for Parasitology 37:243-255
Agusti C, FJ Aznar, PD Olson, DTJ Littlewood and JA Raga. 2005. Morphological and molecular characterization of tetraphyllidean merocercoids of striped dolphins from the western Mediterranean. Parasitology 130:461-474
Bray RA and PD Olson. 2004. The plerocercus of Ditrachybothridium macrocephalum Rees, 1959 from two deep-sea elasmobranches, with a molecular analysis of its position within the order Diphyllidea and a checklist of the hosts of larval diphyllideans. Systematic Parasitology 59:159-167
Reyda FB and PD Olson. 2003. Cestodes of cestodes of Peruvian freshwater stingrays. Journal of Parasitology 89:1018-1024
Brickle P, PD Olson, DTJ Littlewood, A Bishop and A Arkhipkin. 2001. Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetically based identification of their cestode larvae. Canadian Journal of Zoology 79:2289-2296
Olson PD and JN Caira. 2001. Two new species of Litobothrium Dailey, 1969 (Cestoda: Litobothriidea) from thresher sharks in the Gulf of California, Mexico, with redescriptions of two species in the genus. Systematic Parasitology 48:159-177
Olson PD, TR Ruhnke, J Sanney and T Hudson. 1999. Evidence for host-specific clades of tetraphyllidean tapeworms (Platyhelminthes: Eucestoda) revealed by analysis of 18S ssrDNA. International Journal for Parasitology 29:1465-1476
Evolutionarily, the parasitic flatworms were first and foremost parasites of fishes, parasitizing both bony and cartilaginous groups for probably as long as these great lineages have existed. Contemporary sharks and rays are host to an extraordinary parasite fauna, which is especially diverse in cestodes (5 of ~14 orders of cestodes are found exclusively in elasmobranchs).
My interest in these parasites began as a PhD student working with Janine Caira at the University of Connecticut. Janine's group have discovered, documented and studied these parasites for over 20 years and continue to travel the world in pursuit of new fauna.
Evolution of the Trypanorhyncha
Our most recent work in molecular phylogenetics represents 10-years of sampling trypanorhynch diversity around the globe, mostly through the help of collaborators, including Janine, Ian Beveridge, Kirsten Jensen and Robin Overstreet (see Collaborators). These specimens have been characterized both genetically and morphologically and deposited in well-curator museums. The study has revealed a great deal about the interrelationships of the various trypanorhynch lineages, and has shown that there is tremendous plasticity in the form of their tentacular armature, their primary taxonomic features.
Looking at the pattern of their evolution more broadly, we see that the group comprises two main lineages, and by examining the distribution of host associations within these lineages we find a distinct lineage of shark parasites and a distinct lineage of ray parasites. The most parsimonious explanation for this distribution is that sharks and rays themselves followed separate evolutionary paths which resulted in their parasites evolving independently. This overturns the notion that rays are derived from sharks (known as the 'Hypnosqualea' hypothesis; Shirai) and supports recent molecular estimates of elasmobranch evolution.
RELATED PUBLICATIONS:
Palm HW, A Waeschenbach, PD Olson and DTJ Littlewood. 2009. Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 52:351-367
Aznar FJ, C Agusti, DTJ Littlewood, JA Raga and PD Olson. 2007. Insight into the role of cetaceans in the life cycle or tetraphyllideans (Platyhelminthes: Cestoda). International Journal for Parasitology 37:243-255
Agusti C, FJ Aznar, PD Olson, DTJ Littlewood and JA Raga. 2005. Morphological and molecular characterization of tetraphyllidean merocercoids of striped dolphins from the western Mediterranean. Parasitology 130:461-474
Bray RA and PD Olson. 2004. The plerocercus of Ditrachybothridium macrocephalum Rees, 1959 from two deep-sea elasmobranches, with a molecular analysis of its position within the order Diphyllidea and a checklist of the hosts of larval diphyllideans. Systematic Parasitology 59:159-167
Reyda FB and PD Olson. 2003. Cestodes of cestodes of Peruvian freshwater stingrays. Journal of Parasitology 89:1018-1024
Brickle P, PD Olson, DTJ Littlewood, A Bishop and A Arkhipkin. 2001. Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetically based identification of their cestode larvae. Canadian Journal of Zoology 79:2289-2296
Olson PD and JN Caira. 2001. Two new species of Litobothrium Dailey, 1969 (Cestoda: Litobothriidea) from thresher sharks in the Gulf of California, Mexico, with redescriptions of two species in the genus. Systematic Parasitology 48:159-177
Olson PD, TR Ruhnke, J Sanney and T Hudson. 1999. Evidence for host-specific clades of tetraphyllidean tapeworms (Platyhelminthes: Eucestoda) revealed by analysis of 18S ssrDNA. International Journal for Parasitology 29:1465-1476
Scanning electron micrograph of the scolex of a tapeworm of elasmobranchs (Rhinebothrium sp.) | image CJ Healy
Optical 'section' through a mature segment of the stingray tapeworm Anthobothrium sexorchidium (viewed with DIC contrast) | image PD Olson
Scanning electron micrographs of the unsegmented tapeworm Didymobothrium rudolphii. Photos show sections through gravid uterine loops (nb eggs tufted with filaments) | images PD Olson
Taxonomy of parasitic flatworms
EXAMPLE PUBLICATIONS:
Marques J, MJ Santos, DI Gibson, HN Cabral and PD Olson. 2007. Cryptic species of Didymobothrium rudolphii (Cestoda: Spathebothriidea) from the sand sole, Solea lascaris, off the Portuguese coast, with an analysis of their molecules, morphology, ultrastructure and phylogeny. Parasitology 134:1057-1072
Otranto D, S Rebhein, S Weigl, C Cantacessi, A Parisi, R Paolo Lia and PD Olson. 2007. Morphological and molecular differentiation between Dicrocoelium dendriticum (Rudolphi, 1819) and Dicrocoelium orientalis Sudarikov and Ryjkov, 1951 (Platyhelminthes: Digenea). Acta Tropica 104:91-98
Olson PD, DTJ Littlewood, D Griffiths, CR Kennedy and C Arme. 2002. Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. Journal of Helminthology 76:171-174
Olson PD and JN Caira. 2001. Two new species of Litobothrium Dailey, 1969 (Cestoda: Litobothriidea) from thresher sharks in the Gulf of California, Mexico, with redescriptions of two species in the genus. Systematic Parasitology 48:159-177
Scholz T, T Shimazu, PD Olson and K Nagasawa. 2001. Caryophyllidean tapeworms (Platyhelminthes: Eucestoda) from freshwater fishes in Japan. Folia Parasitologica 48:275-288
- Together with NHM curator Emma Sherlock and Claire Healy (Ontario Museum, Canada), we are describing tetraphyllidean species from the blue-spotted stingray Taeniura lymma from the GBR and Borneo
- Circumscription of species of European Mesociestoides using morphometrics and molecules, a Synthesys-sponsored project led by collaborator Gabi Hrckova and assisted by MRes student, Anne O'Connor
EXAMPLE PUBLICATIONS:
Marques J, MJ Santos, DI Gibson, HN Cabral and PD Olson. 2007. Cryptic species of Didymobothrium rudolphii (Cestoda: Spathebothriidea) from the sand sole, Solea lascaris, off the Portuguese coast, with an analysis of their molecules, morphology, ultrastructure and phylogeny. Parasitology 134:1057-1072
Otranto D, S Rebhein, S Weigl, C Cantacessi, A Parisi, R Paolo Lia and PD Olson. 2007. Morphological and molecular differentiation between Dicrocoelium dendriticum (Rudolphi, 1819) and Dicrocoelium orientalis Sudarikov and Ryjkov, 1951 (Platyhelminthes: Digenea). Acta Tropica 104:91-98
Olson PD, DTJ Littlewood, D Griffiths, CR Kennedy and C Arme. 2002. Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. Journal of Helminthology 76:171-174
Olson PD and JN Caira. 2001. Two new species of Litobothrium Dailey, 1969 (Cestoda: Litobothriidea) from thresher sharks in the Gulf of California, Mexico, with redescriptions of two species in the genus. Systematic Parasitology 48:159-177
Scholz T, T Shimazu, PD Olson and K Nagasawa. 2001. Caryophyllidean tapeworms (Platyhelminthes: Eucestoda) from freshwater fishes in Japan. Folia Parasitologica 48:275-288
Molecular Diagnostics
Genetic characterization of flatworm parasites has proven invaluable for matching larval forms with adults (on which most descriptions are based). In turn, this opens up the intermediate form and its unique fauna and environment to questions that have been previously directed solely on adult worms and their definitives hosts. It also has immediate utility in the identification of disease agents in wildlife as well as ourselves.
RELATED PUBLICATIONS:
Aznar FJ, C Agusti, DTJ Littlewood, JA Raga and PD Olson. 2007. Insight into the role of cetaceans in the life cycle or tetraphyllideans (Platyhelminthes: Cestoda). International Journal for Parasitology 37:243-255
Literak I, F Tenora, V Letkova, M Goldova, J Torres and PD Olson. 2006. Mesocestoides litteratus (Batsch, 1786) (Cestoda: Cyclophyllidea: Mesocestoideidae) from the red fox: morphological and 18S rDNA characterization of European isolates. Helminthologia 43:191-195
Garin YJF, M-T Galán-Puchades, A Moulignier, G Robert, F Héran, M Polivka, PD Olson, F Lorenzo, F Derouin and DB Conn. 2005. Case Report: Human brain abscess due to a tetra-acetabulate plerocercoid metacestode (Cyclophyllidea). American Journal of Tropical Medicine and Hygiene 72:513-517
Agusti C, FJ Aznar, PD Olson, DTJ Littlewood and JA Raga. 2005. Morphological and molecular characterization of tetraphyllidean merocercoids of striped dolphins from the western Mediterranean. Parasitology 130:461-474
Olson PD, K Yoder, LF Fajardo L-G, AM Marty, S van de Pas, C Olivier and DA Relman. 2003. Lethal invasive cestodiasis in immunosuppressed patients. The Journal of Infectious Diseases 187:1962-1966
Reyda FB and PD Olson. 2003. Cestodes of cestodes of Peruvian freshwater stingrays. Journal of Parasitology 89:1018-1024
Brickle P, PD Olson, DTJ Littlewood, A Bishop and A Arkhipkin. 2001. Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetically based identification of their cestode larvae. Canadian Journal of Zoology 79:2289-2296
Santamaria-Fries M, LF Fajardo L-G, ML Sogin, PD Olson and DA Relman. 1996. Lethal infection by a previously unrecognized metazoan parasite. The Lancet 347:1797-1801
Genetic characterization of flatworm parasites has proven invaluable for matching larval forms with adults (on which most descriptions are based). In turn, this opens up the intermediate form and its unique fauna and environment to questions that have been previously directed solely on adult worms and their definitives hosts. It also has immediate utility in the identification of disease agents in wildlife as well as ourselves.
RELATED PUBLICATIONS:
Aznar FJ, C Agusti, DTJ Littlewood, JA Raga and PD Olson. 2007. Insight into the role of cetaceans in the life cycle or tetraphyllideans (Platyhelminthes: Cestoda). International Journal for Parasitology 37:243-255
Literak I, F Tenora, V Letkova, M Goldova, J Torres and PD Olson. 2006. Mesocestoides litteratus (Batsch, 1786) (Cestoda: Cyclophyllidea: Mesocestoideidae) from the red fox: morphological and 18S rDNA characterization of European isolates. Helminthologia 43:191-195
Garin YJF, M-T Galán-Puchades, A Moulignier, G Robert, F Héran, M Polivka, PD Olson, F Lorenzo, F Derouin and DB Conn. 2005. Case Report: Human brain abscess due to a tetra-acetabulate plerocercoid metacestode (Cyclophyllidea). American Journal of Tropical Medicine and Hygiene 72:513-517
Agusti C, FJ Aznar, PD Olson, DTJ Littlewood and JA Raga. 2005. Morphological and molecular characterization of tetraphyllidean merocercoids of striped dolphins from the western Mediterranean. Parasitology 130:461-474
Olson PD, K Yoder, LF Fajardo L-G, AM Marty, S van de Pas, C Olivier and DA Relman. 2003. Lethal invasive cestodiasis in immunosuppressed patients. The Journal of Infectious Diseases 187:1962-1966
Reyda FB and PD Olson. 2003. Cestodes of cestodes of Peruvian freshwater stingrays. Journal of Parasitology 89:1018-1024
Brickle P, PD Olson, DTJ Littlewood, A Bishop and A Arkhipkin. 2001. Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetically based identification of their cestode larvae. Canadian Journal of Zoology 79:2289-2296
Santamaria-Fries M, LF Fajardo L-G, ML Sogin, PD Olson and DA Relman. 1996. Lethal infection by a previously unrecognized metazoan parasite. The Lancet 347:1797-1801