| Activities in the Beringian Coevolution Project through 2003:
NSF 0196095 - JA Cook, PI
Field inventories conducted during July and August (1999 to 2003) focused on biodiversity of mammals and associated parasites in Beringia including remote sites in Siberia, Canada, and Alaska. We leveraged considerable logistical support from agencies that manage lands in Alaska, especially the National Park Service. We were also supported by field staff from U of Saskatchewan, U of Alaska, U of New Mexico, Idaho State U, Institute of Biological Problems of the North (Russian Academy of Sciences-Magadan), and Finnish Forest Institute, Vantaa Research Centre-Finland.
Mammals: Across all field seasons, 12,086 mammal specimens (49 species, 31 genera) were captured, based on more than 120,000 trap nights of sampling effort at 126 sites; materials represent geographically extensive and site intensive collections of unprecedented depth and scope. Additionally, significant new series of specimens (e.g., n= 780 from Russia in 2002) resulted from collaboration with trappers and state and federal agencies in Russia, Finland, Alaska and Canada. Each mammal was assigned a unique field identifier, and all tissues, parasites, and other subsamples were linked to the original voucher specimen. Thus materials on divergent pathways could be associated with a specific animal, GPS locality, and date for collection. All mammals sampled were preserved as scientific specimens (skeletal preparations, as whole bodied alcoholics or as dried study skins); survey crews preserved tissues (heart, liver, kidney, spleen, and lung), and embryos in liquid nitrogen. Frozen specimens were deposited in the Alaska Frozen Tissue Collection at the U of Alaska Museum (UAM) and stored at -70°C. Searchable databases (http://arctos.museum.uaf.edu:8080/) at UAM document these collections.
Parasites: Helminth, arthropod and protozoan parasites were a primary focus and we processed, preserved and archived many thousands of lots (a lot represents 1 to several hundreds of specimens including fleas, ticks, mites, coccidia and other protozoan parasites, cestodes, nematodes, and digeneans) from each host. Subsamples of parasites were preserved in appropriate reagents, and frozen in LN2. Protozoans, helminths and arthropods were dispersed to colleagues and collections at the above institutions and at Louisiana State U, Indiana State U, Georgia Southern U, Harvard School of Public Health, and U of Wyoming. Species lists, and preliminary assessment of host associations and biogeographic distribution are in progress for respective components of the parasite fauna. Assessments of descriptive biodiversity (e.g., numerical diversity, abundance, species richness, and overall geographic distribution) will dictate how results based on comparative morphology will be followed by extensive molecular systematic and phylogeographic analyses of parasitic helminths and protozoa. Collaborative efforts and specific and significant outcomes from initial analyses of host-parasite coevolution and historical biogeography are outlined below.
Outcomes: A diverse set of publications (65 in reference section) has been based on BCP collections. In addition, keys and monographs to the Arctic fauna we are studying have been written that are accessible to the general public, wildlife managers and scientists.
Training: Four high school students (2 Native American), 10 undergraduate students (2 Native), 13 graduate students and 4 postdoctoral associates (2 Russian, 1 Canadian) participated in the fieldwork (2 US graduate students were directly supported throughout each year). Students and collaborators have learned modern methods for field inventory in parasitology and mammalogy in the Arctic. Seasoned Arctic biologists (e.g. Cook, Hoberg, Henttonen, MacDonald, Telford) provided field training to students at all levels; museum and laboratory training at UAM, Museum of Southwestern Biology (MSB), and US National Parasite Collection, ARS, USDA continued after the field season. We also helped design and execute a small mammal field project with a high school teacher and his Native students at Noorvik, Alaska. These Yupik Eskimo students won competitions in the Alaska Native High School Science Symposium in 1999 and then attended the National Conference; their project placed second in 2000. Two of these students were members of our field crews in Northwestern Alaska and the class visited UAM to explore the role of museums in natural resource management. Another Native student (Shoshone) from Idaho was a member of a 2003 field expedition. We have delivered a series of public seminars (e.g., to Native communities in Nome), participated in workshops with state and federal agencies (keynote addresses at NPS Inventory Workshops 2000; 2003), and international congresses (plenary lecture and symposia in 2002). Notably, BCP was instrumental to the development of the first two International Workshops for Arctic Parasitology (IWAP) (Saskatchewan, 2000; Rovanemi, Finland, 2003) and is involved in organization of IWAP III to be held in Dawson City, Yukon in 2006.
Maintenance of Database and Website: The majority of host material has been sorted and archived at the University of Alaska Museum with the most recent (2003) collections headed to the Museum of Southwestern Biology. We continue to upgrade the capabilities and accessibility of these data. This collection was the first to link directly to GenBank so that investigators can link directly between a particular specimen and its associated DNA sequences (and vice-versa). Most endo-parasitological materials (and all type specimens) are being catalogued (and entered into the databases) of the US National Parasite Collection (www.anri.barc.usda.gov/bnpcu). Coccidia are accessioned at the University of New Mexico, ticks are in the National Tick Collection at Southern Georgia University, mites are being studied by John Whitaker at Indiana State University and fleas will be archived at the Smithsonian Institution. In addition to the University of Alaska and Museum of Southwestern Biology on-line databases (both part of MANIS), webpages have been developed for the BCP and Coccidia of the World Project (http://biology.unm.edu/biology/coccidia/home.html).
This study (Galbreath & Hoberg) focuses on the hymenolepidid tapeworm fauna of arvicolines. Arostrilepis horrida (previously Hymenolepis horrida) is a widespread and morphologically variable species that occurs in a diversity of voles and lemmings in eastern and western Beringia and more broadly across the Holarctic region. In west Beringia and the adjacent Palearctic, two species (A. beringiensis in Lemmus and A. microtis in Microtis spp.) have been recognized within what is now regarded as a complex of species; they are both poorly differentiated morphologically from A. horrida. The morphological and genetic diversity within this complex has not been adequately assessed, but it holds a key to understanding the intricate faunal history for Beringia. This complex, along with others under study, is critical to examination of the interplay of differing modes and tempos for speciation in Arctic systems driven by both long term isolating events (e.g., the initial opening of Bering Strait), and periodic, cyclical or episodic events associated with alternating stadials and interstadials and habitat fragmentation since the late Pliocene and Pleistocene.
Based on extensive collections, specimens representing Arostrilepis are abundant and common parasites in Clethrionomys rutilus and C. rufocanus, and Microtus spp. but are less commonly found in Synaptomys and Lemmus. Preliminary phylogeographic assessments based on Cyt b sequences now indicate a minimum of 5 host-specific clades of Arostrilepis distributed in Beringia: (1.) A geographically widespread clade (transBeringian) in Clethrionomys spp.; (2.) A geographically restricted clade (limited to the upper Omolon River, Russia) in C. rutilus and C. rufocanus; (3.) A widespread clade in Microtus spp.; (4.) A clade in bog lemmings, Synaptomys; and (5.) A possible clade in Lemmus spp. Unequivocal structural characters are correlated with each of these clades that is defined by divergent sequences. The transBeringian clade in Clethrionomys may be consistent with A. horrida sensu stricto, but requires detailed comparative studies for resolution. Cestodes of the Microtus clade appear consistent with A. microtis, recently described by V. Gulyaev based on specimens from central Siberia; species identity for Beringian materials now requires direct comparisons to Palearctic populations. Cestodes in Lemmus may be consistent with A. beringiensis described by V. Kontrimavichus based on material from Chukhotka. A minimum of 2 undescribed species are represented in these preliminary analyses. We provide for the first time unequivocal evidence that combines both molecular and morphological data, for substantial species-level diversity within A. horrida; previous assessments of diversity have been largely hampered by excessive levels of morphological variation that were problematic in their interpretation.
These insights are significant in expanding our knowledge of parasite biodiversity in Holarctic rodents and in documenting an exceptional level of host specificity within this complex. For example there is no indication of host-switching for respective cestodes in Microtus and Clethrionomys when hosts are in sympatry. Patterns discovered for host-association appear indicative of a deep co-phylogenetic history between hosts and parasites such that respective taxa of arvicolines each may be expected to harbor a restricted fauna. Each of the respective parasite clades is geographically widespread (except the Omolon), suggesting that host-fidelity was maintained during an extensive history of habitat perturbation and cyclical restriction and expansion of ranges for these host-parasite assemblages across Beringia during the Pleistocene. Current evidence suggests that the Omolon clade may be explained in the context of peripheral isolates speciation.
These data are the foundation for an integrated comparative approach to examine the history of Beringia, and its influence on the structure of phylogenetically disparate host-parasite assemblages. Among arvicolines we are in a position to examine an array of parasites with varying life history patterns including both eucestode (e.g., hymenolepidids, anoplocephalids including Paranoplocephala spp.) and nematode taxa (e.g., spirurids such as Riticularia spp., and Mastophorus spp.; trichostrongyles; and lungworms such as Rauschivingylus spp.). Such can contribute important general insights into the role of life history as a determinant of evolutionary rates, the drivers and processes for speciation, and the basis for the evolution of specificity (host specialists versus generalists) in host-parasite systems. Also apparent is a powerful system to explore the role of temporal and geographic scale in the evolution of a complex biota.
Parasites in Sorex spp.
The parasite faunas of insectivores are known to be diverse, and offer an exceptional opportunity to examine the evolution of phylogenetically-related and phylogenetically- disparate parasites in single and related host species. Examination of parasites in single host species allows the variable of host phylogeny to be eliminated as a factor in interpreting rates of divergence in an array of parasite species; it allows the direct examination of the influence of generation time and other parasite life-history traits on patterns of diversification.
Collections at Cantwell, AK in September 1999 were the first to acquire materials for sequence analysis of a diverse array of parasites in Beringian insectivores. A minimum of 8 species of cestodes were collected from 11 S. cinereus (all animals were infected). Preliminary identifications were completed in collaboration with Professor Vladimir Gulyaev, of the Institute of Ecology and Evolution, Novosibirsk, Russia. Hymenolepidid tapeworms included: Staphylocystoides serrula, S. sphenomorphus, Lockerraushcia intricata, Lineolepis pribilofensis, L. lineoloa, an undescribed species of Lineolpis, and Skjabinacanthus falculata. Dilepidid tapeworms include: Monocerus soricis. Subsequent collections in Siberia and Alaska have contributed substantial materials to expand our concepts for host and geographic distribution of a diverse assemblage of helminths in insectivore hosts.
Work in progress includes manuscripts describing and re-describing the Holarctic species represented in the collection along with others that Vladimir Gulyaev (Novosibrsk) has collected in the Palearctic. This will provide a preliminary context for understanding morphological variation and distribution of these parasites in insectivores.
Abomasal parasites in Arctic ruminants.
Following recognition of a cryptic species of abomasal nematode, Teladorsagia boreoarcticus, in Ovibos moschatus and Rangifer tarandus from the central Canadian Arctic (Hoberg et al., 1999), we have accumulated specimens to assess the extent of this complex and relationships of other ostertagiine nematodes in wild ruminants. Collections of abomasal and other parasites have been conducted in far eastern Beringia (MacKenzie Mountains, NWT; Richardson Mtns., NWT; and in the Yukon Territories) in 1999, 2000, and 2001 in collaboration with the Research Group for Arctic Parasitology (RGAP). Current phylogeographic studies focus on a variety of geographic scales (E.P. Hoberg, K. Galbreath, A. Abrams et al., MS In Prep.): (1.) population structure for T. boreoarcticus and Ostertagia gruehneri across the Holarctic; (2.) relationships of mainland and Arctic Island populations of nematodes, evaluating hypotheses for a high Arctic refugium during the Pleistocene; (3.) evaluations of mtDNA diversity in putative populations of O. gruehneri associated with discrete herds of caribou.
Additionally, specimens of Teladorsagia are under study from Dall’s sheep based on comparative morphology and comparative sequence analysis of the ITS and mtDNA. These assessments will contribute to the understanding of the relationships, history and structure of the nematode fauna in Holarctic ruminants. Comparative morphological studies suggest an additional new and cryptic species of Teladorsagia in Ovis dalli.
Significant orphan collections from wild sheep, and caribou held in the Canadian Museum of Nature, and at the University of Alaska, Fairbanks have also been under re-evaluation since November 2000. These will contribute to a substantial knowledge of parasite biodiversity in the Holarctic. Collectively these materials have contributed to a broader understanding of the diversity of strongylate nematodes in North American ruminants (Hoberg, Kocan and Rickard, 2001).
Lungworms and muscleworms in ruminants.
In collaboration with the RGAP, we have also been focusing on the systematics and biogeography of protostrongylid nematodes in Ovis dalli. In large part, these studies originated following the discovery of Umingmakstrongylus, a new genus of lungworm in endemic muskoxen of the Central Canadian Arctic and the need to understand its relationships and biogeography (Kutz, Hoberg and Polley, 2001; Carreno and Hoberg, 1999). Our recent studies have provided the first definitive collections and identification of Parelaphostongylus cf. odocoilei, and Protostrongylus stilesi in the Northwest Territories and Alaska (Kutz et al., 2001). Collections in 2000 and 2001 resulted in identification of P. odocoilei and both new host and geographic records in both Dall’s sheep and Mountain Goat from the Chugach Mountains, Alaska. Analyses of mtDNA and ITS-2 sequences have also contributed to our understanding of structural polymorphism in larval P. odocoilei, and have resolved the question of species identity of Parelaphostrongylus in Subarctic thinhorn sheep (E. Jenkins, E.P. Hoberg et al., MS In Prep.)
An apparent contact zone for muskoxen and Dall’s sheep in eastern Alaska and the Yukon Territory has been the driver for host-switching by P. stilesi from the latter host. This is a significant finding as it indicates the strong ecological basis for apparent specificity and host distribution for some parasites, and suggests the potential for ecological disruption in the context of global change (Hoberg et al. 2002). Further, phylogeographic studies of P. stilesi are designed to examine a history of host isolation during the post-Pleistocene period in the Brooks Range, Richardson Mountains, and the Mackenzie Mountains in eastern Beringia.
Distribution, status and phylogeographic analyses of mammalian hosts.
A series of papers by Cook, MacDonald and collaborators have focused on the historical biogeography, status and distribution of Beringian mammals. Other studies (including 7 master’s or doctoral theses in progress) are underway. A primary contribution will be a book entitled “The Mammals of Alaska”, a work that has not previously been completed for this important high latitude region.
Beringian history and the marine fauna.
Phylogenetic studies of marine host parasite systems contribute to a broader context for addressing the history of Beringia. Cospeciation and biogeographic analyses of flatworms in pinnipeds has led to a refinement of the Arctic Refugium Hypothesis that addresses the patterns and processes for diversification in complex host-parasite assemblages across the Beringian region and the Pacific and Arctic basins (Hoberg and Adams, 2000).
General biodiversity studies.
Aside from collections oriented activities of the BCP, significant reviews on the role and impact of parasitology in biotic survey and inventory (Brooks and Hoberg, 2000, 2001) and historical biogeography (Hoberg and Klassen, In Press) were completed. These papers discussed the powerful conceptual foundation from parasitology that links ecology, systematics, evolution and biogeography. Additionally, a position paper was developed on the integration of biodiversity, parasitology, research collections and informatics (Hoberg In Press).
Hoberg EP. Phylogeny, history and biodiversity: Understanding faunal structure and biogeography in the marine realm. Ecological Parasitology on the Turn of the Millennium. Zoological Institute, Russian Academy of Sciences & Scandinavian Society for Parasitology, St. Petersburg, Russia. July 2000.
Hoberg EP. Biodiversity and Biogeography: Establishing the context and keystones for Arctic parasitology. General Introduction. International Workshop for Arctic Parasitology, Prince Albert National Park, Saskatchewan, Canada. October 2000.
Kutz S, Hoberg EP, Polley L. Global warming and host-parasite systems in the Arctic: Should we be concerned? Issues Presentation. International Workshop for Arctic Parasitology, Prince Albert National Park, Saskatchewan, Canada. October 2000.
Jenkins E, Hoberg EP, Kutz S, Veitch A, Polley L. Challenges in investigating protostrongylids in northern hosts: Parelaphostrongylus odocoilei in Dall's sheep (Ovis dalli dalli) of northern North America. Issues Presentation. International Workshop for Arctic Parasitology, Prince Albert National Park, Saskatchewan, Canada. October 2000.
Hoberg EP. Foundations for an integrative parasitology: collections archives and biodiversity informatics. Helminthological Society of Washington, 676th Meeting, and Smithsonian Institution, Symposium- Parasitology in Science and Society. Washington D.C. 27 October 2001.
Cook J, Galbreath K, Runck A, Federov V, Hoberg EP. Beringian Coevolution Project: An interface between mammalogy and parasitology. Biogeography and Evolution in Northern Host-Parasite Systems: A Symposium Honoring Robert L. Rausch and Virginia R. Rausch. International Congress of Parasitology (ICOPA) X. Vancouver, Canada. 4-9 August 2002.
Hoberg EP. Colonization and diversification: Historical and coevolutionary trajectories among cestodes, cetaceans and pinnipeds. Symposium for Parasites of Marine Mammals. ICOPA X. Vancouver, Canada. 4-9 August 2002.
Hoberg EP, Kutz SJ, Cook J. Arctic biodiversity: From discovery to faunal baselines- revealing the history of a dynamic ecosystem. SubPlenary Lecture, in Parasitology and Biodiversity in an Age of Discovery. ICOPA X. Vancouver, Canada. 4-9 August 2002.
Hoberg EP. Robert and Virginia Rausch: Fifty years on the frontiers of northern parasitology. Biogeography and Evolution in Northern Host-Parasite Systems: A Symposium Honoring Robert L. Rausch and Virginia R. Rausch. International Congress of Parasitology X. Vancouver, Canada. 4-9 August 2002.
Contributed Papers (with abstracts)
Galbreath, K., and J. Cook. 2001. Phylogeography of the tundra vole (Microtus oeconomus) in Beringia. June - American Society of Mammalogists annual meeting, Missoula, MT.
Goethert HK, Telford SR III. Beta-tubulin sequence polymorphism as
Goethert HK, Lance E, Cook JA, Telford SR III. Prevalence and genetic
Kutz S, Hoberg EP, Polley L. Parasite biodiversity, development and transmission: An integrative model for monitoring climate change at northern latitudes. 12th Northern Wild Sheep and Goat Conference, Whitehorse, Yukon Territory, Canada. May 2000.
Kutz S, Veitch A, Hoberg EP, Elkin B, Jenkins E, Polley L. New host and geographic records for Protostrongylus stilesi and Parelaphostrongylus odocoilei in Dall's sheep from the Mackenzie Mountains, NWT. 12th Northern Wild Sheep and Goat Conference, Whitehorse, Yukon Territory, Canada. May 2000.
Kutz SJ, Hoberg EP, Polley L. A model for investigating the development, transmission, and response to climate change of protostrongylid parasites on the Arctic tundra. Wildlife Disease Association, Annual Meeting. Jackson, Wyoming. 4-8 June 2000.
Kutz SJ, Veitch A, Jenkins E, Elkin B, Chirino-Trejo M, Hoberg E, Polley L. Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall's sheep: Predisposing factors for mortality? Wildlife Disease Association, Annual Meeting. Jackson, Wyoming. 4-8 June 2000.
Hoberg EP, Rosenthal B. Biosystematics and faunal assessment of parasites in Holarctic Bovidae and Cervidae. Information Exchange. International Workshop for Arctic Parasitology, Prince Albert National Park, Saskatchewan, Canada. 1-4 October 2000.
Galbreath K, Hoberg EP, Telford S, Cherniavsky F, Kutz S, Duszynski D, Waltari E, Cook J. Current status of the Beringian Coevolution Project. Information Exchange. International Workshop for Arctic Parasitology, Prince Albert National Park, Saskatchewan, Canada. October 2000.
Kutz S, Jenkins E, Elkin B, Hoberg EP. Research in wildlife parasitology in the Northwest Territories and Yukon. Information Exchange. International Workshop for Arctic Parasitology, Prince Albert National Park, Saskatchewan, Canada. October 2000.
Runck, A., E. Lessa, J. Cook. 2002. Accelerated replacement ratios in diving pinnipeds and cetaceans in the cytochrome b gene. American Genetics Association Annual Meeting, Tempe AZ
Stone, K. D. and J. A. Cook. 2000. Phylogeography of American martens
Stone, K. D., R. W. Flynn and J. A. Cook. 2000. Genetic relationships
among marten populations of Southeast Alaska. Presented at: The 10th
Stone, K. D. and J. A. Cook. 2000. Interpopulation divergence of American pine marten (Martes americana). Presented at: Alaska Cooperative Fish & Wildlife Research Unit meeting in Fairbanks, Alaska.
Hoberg EP, Kutz SJ. Arctic biodiversity: baselines, archives and host-parasite systems as a window on faunal change. Taxonomy, Systematics, Phylogeny. American Society of Parasitologists, 76th Annual Meeting, Albuquerque, New Mexico. June 2001.
Kutz SJ, Veitch A, Nagy J, Elkin B, Hoberg EP, Jenkins E, Polley L. Contact zones between expanding muskoxen populations and Dall's sheep- An emerging disease issue.13th Biennial Northern Wild Sheep and Goat Council Symposium. Rapid City, South Dakota. April 2002.
Jenkins E, Veitch A, Hoberg EP, Kutz SJ, Elkin B, Polley L. Distribution, life cycle and significance of Parelaphostrongylus odocoilei in a new host- Thinhorn sheep. 13th Biennial Northern Wild Sheep and Goat Council Symposium. Rapid City, South Dakota. April 2002.
Kutz SJ, Veitch A, Simmons N, Hoberg EP, Elkin B, Jenkins E, Polley L. Parasites in Dall's sheep: What can we learn from historical and contemporary collections (Or: Putting together the pieces).13th Biennial Northern Wild Sheep and Goat Council Symposium. Rapid City, South Dakota. April 2002.
Jenkins E, Veitch A, Hoberg EP, Kutz S, Elkin B, Polley L. Life cycle, distribution and significance of Parelaphostrongylus odocoilei in thinhorn sheep (Ovis dalli).World Conference on Mountain Ungulates III. Zaragosa, Spain. June 2002.
Kutz SJ, Nagy J, Elkin B, Hoberg EP, Wagner B, Polley L. Epidemiology of abomasal parasites of muskoxen on Banks Island, Northwest Territories. World Conference on Mountain Ungulates III. Zaragosa, Spain. June 2002.
Kutz SJ, Veitch A, Simmons N, Hoberg EP, Elkin B, Jenkins E, Polley L. Parasites in Dall's sheep: What can we learn from historical and contemporary collections? World Conference on Mountain Ungulates III. Zaragosa, Spain. June 2002.
Kutz SJ, Hoberg EP, Cook J, Simmons N, Nagy J, Veitch A, Elkin B, Polley L. Parasitism in wildlife populations: Baselines, biodiversity and monitoring in the Arctic. Wildlife Parasitology Session, International Congress of Parasitology X. Vancouver, Canada. 4-9 August 2002.
Invited Lectures (without abstracts)
Hoberg EP.1999. Arctic biodiversity: History, biogeography and coevolution in ruminant parasite systems. University of Alaska Museum, Fairbanks, AK. September 1999.
Cook, JA. 1999. "Historical biogeography of North American mammals: Evidence for multiple lineages across Alaska and the North Pacific Coast." University of Washington, Dept. of Zoology.
Cook, JA. 2000. "Multiple mammalian lineages along the North Pacific Coast suggest a complex environmental history" University of California, Davis, May
Cook, JA. 2000. "Historical Biogeography of Northwestern North America: A Mammalian Perspective", Idaho State University, Pocatello, April,
Cook, JA. 2000. "Comparative phylogeography of the North Pacific Coast". Ohio University, Athens, January
Hoberg EP. 2000. Historical biogeography and coevolution in marine systems: Perspectives from pinnipeds and parasites. Dept. of Zoology, University of Bergen, Norway, June 2000.
Hoberg EP. 2000. Marine biodiversity: Patterns of biocomplexity in a bipolar world. Dept. of Biology, Gettysburg College, Pennsylvania. 9 November 2000.
Hoberg EP, Kutz SJ. Arctic biodiversity: Baselines, archives, biological collections and host-parasite systems as a window on faunal change. Canadian Museum of Nature, 2000 Seminar Series, Ottawa, Canada. 15 November 2000.
Kutz S, Hoberg EP. Parasites as components of northern ecosystems: A proposal for long-term monitoring. Department of Resources, Wildlife & Economic Development (DRWED), Govt. of the Northwest Territories. Yellowknife, NT. 15 December 2000.