Mitochondrial DNA and microsatellite DNA variation in domestic reindeer (Rangifer tarandus tarandus) and relationships with wild caribou (Rangifer tarandus granti, Rangifer tarandus groenlandicus, and Rangifer tarandus caribou)

Reindeer (Rangifer tarandus tarandus) in Alaska are semidomestic livestock descended from 1280 animals introduced from Siberia, Russia, approximately 100 years ago. Genetic variation at 18 microsatellite DNA loci and the cytochrome b gene of mitochondrial DNA (mtDNA) was quantified in reindeer from Alaska, Siberia (Russia), and Scandinavia and compared with wild North American caribou. Mean sequence divergence among 15 mtDNA haplotypes in reindeer was 0.007 substitutions per nucleotide site, and reindeer mtDNA is polyphyletic with caribou mtDNA. Microsatellite allele and mtDNA haplotype frequencies are similar between Alaskan and Russian reindeer and differentiated between these and Scandinavian reindeer. The frequencies of microsatellite alleles and mtDNA haplotypes are different in reindeer and wild caribou (Rangifer tarandus granti, Rangifer tarandus groenlandicus, and Rangifer tarandus caribou). Alaskan reindeer have maintained a genetic variation comparable to that in Russia and differentiated from that of wild caribou, >100 years after their introduction to Alaska.     

Parelaphostrongylus odocoilei (Nematoda: Protostrongylidae) and a protostrongylid nematode in woodland caribou (Rangifer tarandus caribou) of Alberta, Canada

Two size-groups of dorsal-spined, first-stage, nematode larvae were found in feces of woodland caribou, Rangifer tarandus caribou (Gmelin), in Alberta from 1976-1982. Larvae from caribou feces in northeastern Alberta were 451 +/- 17 micrograms in length, while those from west-central Alberta were 362 +/- 18 micrograms in length. Larvae collected from west-central Alberta developed to the infective stage, experimentally, in the terrestrial gastropod Triodopsis multilineata (Say) and were infective to captive mule deer fawns, Odocoileus H. hemionus (Rafinesque). Adult nematodes, identified as Parelaphostrongylus odocoilei (Hobmaier and Hobmaier, 1934), were recovered from the skeletal muscles of the mule deer.     

Genetic variation in caribou and reindeer (Rangifer tarandus)

Genetic variation at seven microsatellite DNA loci was quantified in 19 herds of wild caribou and domestic reindeer (Rangifer tarandus) from North America, Scandinavia and Russia. There is an average of 2.0-6.6 alleles per locus and observed individual heterozygosity of 0.33-0.50 in most herds. A herd on Svalbard Island, Scandinavia, is an exception, with relatively few alleles and low heterozygosity. The Central Arctic, Western Arctic and Porcupine River caribou herds in Alaska have similar allele frequencies and comprise one breeding population. Domestic reindeer in Alaska originated from transplants from Siberia, Russia, more than 100 years ago. Reindeer in Alaska and Siberia have different allele frequencies at several loci, but a relatively low level of genetic differentiation. Wild caribou and domestic reindeer in Alaska have significantly different allele frequencies at the seven loci, indicating that gene flow between reindeer and caribou in Alaska has been limited.     

Experimental oral transmission of chronic wasting disease to reindeer (Rangifer tarandus tarandus)

Chronic wasting disease (CWD), a transmissible spongiform encephalopathy of cervids, remains prevalent in North American elk, white-tailed deer and mule deer. A natural case of CWD in reindeer (Rangifer tarandus tarandus) has not been reported despite potential habitat overlap with CWD-infected deer or elk herds. This study investigates the experimental transmission of CWD from elk or white-tailed deer to reindeer by the oral route of inoculation. Ante-mortem testing of the three reindeer exposed to CWD from white-tailed deer identified the accumulation of pathological PrP (PrP(CWD)) in the recto-anal mucosa associated lymphoid tissue (RAMALT) of two reindeer at 13.4 months post-inoculation. Terminal CWD occurred in the two RAMALT-positive reindeer at 18.5 and 20 months post-inoculation while one other reindeer in the white-tailed deer CWD inoculum group and none of the 3 reindeer exposed to elk CWD developed disease. Tissue distribution analysis of PrP(CWD) in CWD-affected reindeer revealed widespread deposition in central and peripheral nervous systems, lymphoreticular tissues, the gastrointestinal tract, neuroendocrine tissues and cardiac muscle. Analysis of prion protein gene (PRNP) sequences in the 6 reindeer identified polymorphisms at residues 2 (V/M), 129 (G/S), 138 (S/N) and 169 (V/M). These findings demonstrate that (i) a sub-population of reindeer are susceptible to CWD by oral inoculation implicating the potential for transmission to other Rangifer species, and (ii) certain reindeer PRNP polymorphisms may be protective against CWD infection.     

Molecular characterization of Cryptosporidium sp. isolated from northern Alaskan caribou (Rangifer tarandus)

Cryptosporidium sp. was found in 3 out of 49 caribou (Rangifer tarandus) from northern Alaska. Segments of both the 18S ribosomal RNA and the heat shock protein genes were amplified from the caribou isolate and compared with that obtained from an isolate from a wild white-tailed deer (Odocoileus virginianus) in Virginia as well as other species and isolates available from GenBank. Analyses showed the white-tailed deer isolate to be identical with the C. parvum cattle genotype; however, the caribou isolate represents a new genotype closely related to C. serpentis, C. muris, and C. andersoni. Giardia sp. was not detected in any of the caribou samples nor was Cryptosporidium sp. or Giardia sp. detected in any of the 42 moose (Alces alces) samples examined.     

Prevalence of Toxoplasma gondii antibodies in barren-ground caribou (Rangifer tarandus groenlandicus) from the Canadian Arctic

Prevalence of antibodies to Toxoplasma gondii was determined in 147 barren-ground caribou (Rangifer tarandus groenlandicus) from 5 herds in the Northwest Territories and Nunavut, northern Canada, by the modified agglutination test (MAT). In the mainland herds (Bluenose, Bathurst, and Beverly), antibodies were found in 43 (37%) of 117 caribou, and MAT titers were 1:25 in 10, 1:50 in 24, and 1:500 in 9. In the island herds, only 1 (4.3%) of 23 animals sampled from the North Baffin Island herd was positive (titer = 1:25) and no antibodies were detected in 7 caribou from the Dolphin and Union herd. The high prevalence of antibodies to T. gondii in the mainland caribou herds indicates that caribou meat may contain viable T. gondii.     

Antler stiffness in caribou (Rangifer tarandus): testing variation in bone material properties between males and females

Vertebrate bones, including deer antler, often exhibit variation in their mechanical properties that corresponds to differences in the functional demands they encounter. Among deer, antlers are found in both males and females only in caribou (Rangifer tarandus). Several differences between male and female R. tarandus in behavior and physiology might subject their antlers to differing demands, potentially making divergence of antler material properties between the sexes advantageous. Alternatively, antler material properties might not differ between male and female R. tarandus because both sexes are members of the same species, and the properties of their antlers could, therefore, have emerged under similar pressures and constraints through evolution. To test for sexual dimorphism in antler material properties, we compared the stiffness (Young's modulus of elasticity) of antler specimens from male and female caribou using three-point bending tests. Despite behavioral and physiological differences between males and females, stiffness values did not differ significantly between the sexes in caribou, with a mean (+/-S.E.) stiffness of 5.8+/-0.4GPa across all specimens. This value differed by less than 10% from the values published for R. tarandus specimens of unknown sex, verifying the comparability of bone material property data collected across multiple studies, and lending confidence to recent analyses of the evolution of antler stiffness in deer that have drawn on literature data.     

Serum biochemistry, serology, and parasitology of boreal caribou (Rangifer tarandus caribou) in the Northwest Territories, Canada

Boreal caribou (Rangifer tarandus caribou) are an ecologically and culturally important wildlife species and now range almost exclusively in the boreal forests of Canada, including the Northwest Territories, northern Alberta, and British Columbia. Boreal caribou are threatened throughout their Canadian range because of direct and indirect natural and anthropogenic factors. In the Northwest Territories, however, they have a continuous range that overall has not yet been subjected to the same degree of anthropogenic habitat fragmentation and degradation that has occurred elsewhere in Canada. To monitor the health of boreal caribou populations and individuals, we collected blood from 104 adult, female boreal caribou captured between March 2003 and February 2006 and measured serum biochemical parameters. Serum creatinine was higher in pregnant than in nonpregnant caribou. Several biochemical parameters differed among years, but they tended to be similar to those reported for reindeer. Serum antibodies were found to an alphaherpesvirus, Toxoplasma gondii, and to the Mycobacterium avium subspecies paratuberculosis in 37.5, 2.9, and 1.3% of boreal caribou, respectively. Fecal samples were collected from 149 boreal caribou, and Cryptosporidium sp. oocysts, Giardia sp. cysts, trichostrongyle ova, dorsal-spined nematode larvae, cestode ova, and Eimeria sp. were found. Trypanosoma sp. was detected in the blood of 72.1% of boreal caribou. Eimeria sp., Cryptosporidium sp., and Giardia sp. have not been previously reported in boreal caribou.     

Survival in the Rockies of an endangered hybrid swarm from diverged caribou (Rangifer tarandus) lineages

In North America, caribou ( Rangifer tarandus ) experienced diversification in separate refugia before the last glacial maximum. Geographical isolation produced the barren-ground caribou ( Rangifer tarandus groenlandicus ) with its distinctive migratory habits, and the woodland caribou ( Rangifer tarandus caribou ), which has sedentary behaviour and is now in danger of extinction. Herein we report on the phylogenetics, population structure, and migratory habits of caribou in the Canadian Rockies, utilizing molecular and spatial data for 223 individuals. Mitochondrial DNA analyses show the occurrence of two highly diverged lineages; the Beringian–Eurasian and North American lineages, while microsatellite data reveal that present-day Rockies' caribou populations have resulted from interbreeding between these diverged lineages. An ice-free corridor at the end of the last glaciation likely allowed, for the first time, for barren-ground caribou to migrate from the North and overlap with woodland caribou expanding from the South. The lack of correlation between nuclear and mitochondrial data may indicate that different environmental forces, which might also include human-caused habitat loss and fragmentation, are currently reshaping the population structure of this postglacial hybrid swarm. Furthermore, spatial ecological data show evidence of pronounced migratory behaviour within the study area, and suggest that the probability of being migratory may be higher in individual caribou carrying a Beringian–Eurasian haplotype which is mainly associated with the barren-ground subspecies. Overall, our analyses reveal an intriguing example of postglacial mixing of diverged lineages. In a landscape that is changing due to climatic and human-mediated factors, an understanding of these dynamics, both past and present, is essential for management and conservation of these populations.     

Dermacentor albipictus (Acari, Ixodidae) on captive reindeer and free-ranging woodland caribou

Infestations of winter ticks (Dermacentor albipictus) on two captive reindeer (Rangifer tarandus tarandus) are reported and may be associated with increased grooming and alopecia. Over 400,000 ticks were recovered from one reindeer. Few ticks (less than 25 ticks/animal) were found on three free-ranging woodland caribou (Rangifer tarandus caribou).     

Population genetics of the native caribou (Rangifer tarandus groenlandicus) and the semi-domestic reindeer (Rangifer tarandus tarandus) in Southwestern Greenland: Evidence of introgression

Over the past centuries the native caribou ofWest Greenland has gone through extensive population size fluctuations, with reductionsas great as 90% in less than 20 years.Norwegian semi-domestic reindeer wereintroduced to the Nuuk area in 1952 because ofthe small number of caribou in Greenland.Although the reindeer and caribou wereinitially kept separated, mixing has occurredsince the 1970's. We investigated the genotypicstructure of caribou and reindeer in South-westGreenland, using five polymorphicmicrosatellite markers isolated from cattle,sheep, goat and red deer. A total of ninetysamples were collected, which included samplesfrom caribou of four different regions andsamples from two different reindeer herds.Based on the genetic variation of the fivemarkers, our results shows that the caribou andthe reindeer populations in the six regionssampled are genetically differentiated withineach group and the two subspecies aredifferentiated from each other. A likelyexplanation for the genetic isolation of thepopulations investigated is that naturalbarriers (glaciers and wide fjords) exists inthe area. Furthermore we found that introducedNorwegian domestic reindeer hybridized with thenative Greenlandic caribou in two areasneighbouring Nuuk.     

Evidence of alphaherpesvirus infections in Alaskan caribou and reindeer

Background  

The reindeer (Rangifer tarandus tarandus) industry in Alaska began with animals imported from Siberia (Russia) in the 1890's. Cervid herpes virus 2 (CvHV2) is endemic in reindeer in Scandinavia. We sought to determine if the same virus, or similar herpesviruses, were circulating in Alaskan reindeer and caribou (Rangifer tarandus granti). Serum samples from 292 reindeer were collected during annual reindeer handlings (1988-2005) near Nome, Alaska. In 2005, swab samples were collected from 40 calves from this herd, near Nome, Alaska. In 2007, ocular and nasal swab samples were collected from 30 apparently healthy reindeer calves near Wales, Alaska. Samples of plasma and white blood cells were collected from three Alaskan caribou herds, Mulchatna (n = 24), Teshekpuk (n = 34) and the Western Arctic (n = 87) in 2009.     

Panting in reindeer (Rangifer tarandus)

Two winter-insulated Norwegian reindeer (Rangifer tarandus tarandus) were exposed to air temperatures of 10, 20, 30, and 38 degrees C while standing at rest in a climatic chamber. The direction of airflow through nose and mouth, and the total and the nasal minute volumes, respectively, were determined during both closed- and open-mouth panting. The animals alternated between closed- and open-mouth panting, but the proportion of open-mouth panting increased with increasing heat load. The shifts from closed- to open-mouth panting were abrupt and always associated with a rise in respiratory frequency and respiratory minute volume. During open-mouth panting, the direction of airflow was bidirectional in both nose and mouth, but only 2.4 +/- (SD) 1.1% of the air was routed through the nose. Estimates suggest that the potential for selective brain cooling is markedly reduced during open-mouth panting in reindeer as a consequence of this airflow pattern.     

Hearing in reindeer (Rangifer tarandus)

The audiogram of two yearling male reindeer (Rangifer tarandus tarandus) were determined using a conditioned suppression/avoidance procedure. During testing, the animal was drinking from a metal bowl while pure tone signals were played at random intervals and followed by an electric shock in the bowl. By breaking contact with the bowl at sound signals, the animal avoided the shock. The animals detected sounds at intensities of 60 dB or less from 70 Hz to 38 kHz. The frequency range of best sensitivity was relatively flat from 1 kHz to 16 kHz, with a best sensitivity of 3 dB at 8 kHz. The hearing ability of reindeer is similar to the hearing ability of other ungulates.     

Trypanosoma cervi from Alaskan Reindeer,Rangifer tarandus1

Twenty-nine (64.4%) of 45 reindeer, Rangifer tarandus, examined over a two-year period were infected with trypanosomes. Trypomastigotes and dividing epimastigotes were found in the blood of fawns, cows, and bulls. Morphometric analysis of bloodstream trypomastigotes from reindeer and comparison of these parasites with similar stages of trypanosomes from elk, mule deer, and white-tailed deer from the contiguous United States proved them conspecific; the trypanosomes from these members of the Cervidae are identified as Trypanosoma cervi Kingston & Morton, 1975. This is the first report of trypanosomes from reindeer. No pathogenic effects are known to be caused by these parasites.     

Experimental Fascioloides magna infections of mule deer (Odocoileus hemionus hemionus).

Six mule deer (Odocoileus hemionus hemionus) and one white-tailed deer (Odocoileus virginianus), approximately 5-mo-old, each were inoculated orally with 500 metacercariae of Fascioloides magna. All mule deer died from liver fluke infection between 69 and 134 days (mean = 114, SE = 9.9) after inoculation. Between 38 and 326 immature F. magna (mean = 102, SE = 45.5) were recovered from each deer at necropsy. Flukes were present in livers, lungs, and free in pleural and peritoneal spaces. Infection was characterized by necrotizing hepatitis, fibrosing peritonitis and pleuritis, and hematin pigment accumulation in liver, lung, and many other internal organs. Eggs of F. magna first were detected in feces of the white-tailed deer 28 wk after inoculation, and weekly thereafter until the healthy deer was euthanized at 31 wk. At necropsy, 205 F. magna, including 12 encapsulated mature and 193 nonencapsulated immature flukes were recovered from liver, lungs, and free in abdominal and thoracic spaces of the white-tailed deer. Based on these results, F. magna may be fatal to mule deer within 5 mo of infection. Like domestic sheep and goats, mule deer may be highly susceptible to infection, and it is unlikely mule deer can survive infection with large numbers of F. magna.     

Changing northern vegetation conditions are influencing barren ground caribou (Rangifer tarandus groenlandicus) post‐calving movement rates

Aim

To quantify changes in vegetation productivity over the past three decades across five barren ground caribou (Rangifer tarandus groenlandicus) herd ranges and assess how these changes are influencing caribou movement rates.

Location

Northwest Territories and Nunavut, Canada.

Methods

As an indicator of vegetation productivity, the enhanced vegetation index (EVI) was calculated on newly developed cloud‐free, gap‐free, Landsat surface reflectance image composites representing 1984–2012. Changes in EVI were assessed on a pixel basis using Theil‐Sen's nonparametric regression and compared across herd ranges and land cover types using generalized least squares regression. Animal movement velocity was calculated from caribou telemetry data and generalized additive mixed models were used to link movement rates with vegetation productivity during the post‐calving phase of the year (July and August).

Results

Vegetation productivity increased across the five caribou herd ranges examined. The largest productivity increase occurred over the ranges of the most western herds, with the largest observed changes in grassland or shrub habitats. Caribou tended to move more slowly through tundra habitats with elevated levels of productivity to a point, while grasslands movement rates decreased linearly with increasing productivity. Movement velocities peaked at intermediate productivity levels in shrub habitats.

Main conclusions

Over the three decades of collected data, barren ground caribou habitats have become more productive, which is consistent with other studies that have documented increases in Arctic vegetation productivity. The more western herds, whose ranges are also closest to the Arctic Ocean, experienced the largest increases in productivity. Finally, we demonstrate that barren ground caribou movement patterns will likely change as a result of changing vegetation productivity in complex manners depending on herd, habitat type and the magnitude of change in vegetation productivity.     

Prion protein genes in caribou from Alaska

Prion protein genes were sequenced in free-ranging Alaska caribou (Rangifer tarandus grantii). Caribou prion alleles are identical or nearly so to those of wapiti, white-tailed deer, and mule deer. Five single-nucleotide polymorphisms were detected with substitutions at residues 2 (V-->M), 129 (G-->S), 138 (S-->N), 146 (N-->N), and 169 (V-->M). The 138N codon had been previously reported only in prion pseudogenes of other cervids. In caribou, the 138S and 138N alleles are present at frequencies of approximately 0.7 and 0.3, respectively, and they are seen in both homozygotes and heterozygotes of three geographically separated herds, each a component of the continental metapopulation. Genetics seems to permit the spread of chronic wasting disease from middle-latitude deer to high-latitude caribou in North America.     

The primary structure of hemoglobin from reindeer (Rangifer tarandus tarandus) and its functional implications

The primary structures of alpha- and beta-chains of hemoglobin from reindeer (Rangifer tarandus tarandus) were determined. Comparison of the reindeer hemoglobin sequence with those of human and bovine hemoglobins showed 50 and 29 substitutions per alpha beta dimer, respectively. The influence of replacements on the modulation of hemoglobin oxygen affinity by heterothopic ligands and temperature, as well as their importance on the structure-function relationships in hemoglobin are discussed.