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.     

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.     

Genetic variation in domestic reindeer and wild caribou in Alaska

Reindeer ( Rangifer tarandus tarandus ) were introduced into Alaska 100 years ago and have been maintained as semidomestic livestock. They have had contact with wild caribou ( R. t. granti ) herds, including deliberate crossbreeding and mixing in the wild. Reindeer have considerable potential as a domestic animal for meat or velvet antler production, and wild caribou are important to subsistence and sport hunters. Our objective was to quantify the genetic relationships of reindeer and caribou in Alaska. We identified allelic variation among five herds of wild caribou and three herds of reindeer with DNA sequencing and restriction enzymes for three loci: a DQA locus of the major histocompatibility complex ( Rata-DQA1 ), K-casein and the D-loop of mitochondrial DNA. These loci are of interest because of their potential influence on domestic animal performance and the fitness of wild populations. There is considerable genetic variation in reindeer and caribou for all three loci, including five, three and six alleles for DQA , K-casein and D-loop respectively. Most alleles occur in both reindeer and caribou, which may be the result of recent common ancestry or genetic introgression in either direction. However, allele frequencies differ considerably between reindeer and caribou, which suggests that gene flow has been limited.     

An epizootic of besnoitiosis in captive caribou (Rangifer tarandus caribou), reindeer (Rangifer tarandus tarandus) and mule deer (Odocoileus hemionus hemionus)

Besnoitia sp. was diagnosed in two caribou (Rangifer tarandus caribou) which died of pneumonia at the Assiniboine Park Zoo (Winnipeg, Manitoba, Canada) in 1983. During the following 3 yr besnoitiosis spread to an isolated herd of caribou, to mule deer (Odocoileus hemionus hemionus) and to reindeer (Rangifer tarandus tarandus). Reduction of exposure to biting insects appears to have reduced the transmission of besnoitiosis within the reindeer herd. The morbidity rate was approximately 82% in caribou and 67% in mule deer over the age of 2 mo. Most animals with clinical signs were euthanized; this precluded an estimation of the disease-related mortality rate. Twenty-eight caribou, 10 mule deer and three reindeer have been euthanized or died as a result of this epidemic. Attempts to artificially transmit the disease to potentially susceptible intermediate and definitive hosts were unsuccessful.     

Polymorphism of the mtDNA control region in wild reindeer Rangifer tarandus (Mammalia: Artioodactyla) from the European part of Russia

Genetic diversity of wild reindeer (Rangifer tarandus) inhabiting the European part of Russia, including Komi Republic, Arkhangelsk oblast, Murmansk oblast, and the Republic of Karelia was characterized using sequence polymorphism of the mtDNA control region. Despite of currently low population number of wild reindeer, they were characterized by a high level of genetic diversity (?? = 0.018; H = 0.872 to 0.914). Phylogenetic analysis showed close relationships between European reindeer and wild reindeer of Siberia. In reindeer from Murmansk oblast a haplotype in common with the wild reindeer form Southwestern Norway was described. The reindeer sample examined contained no haplotypes earlier described for the reindeer of Central Norway. It is suggested that in recent past wild reindeer from the European north of Russia formed one population with the reindeer from the north of the Asian part of Eurasia.     

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.     

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).     

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.     

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.     

Reconstruction of caribou evolutionary history in Western North America and its implications for conservation

The role of Beringia as a refugium and route for trans-continental exchange of fauna during glacial cycles of the past 2million years are well documented; less apparent is its contribution as a significant reservoir of genetic diversity. Using mitochondrial DNA sequences and 14 microsatellite loci, we investigate the phylogeographic history of caribou (Rangifer tarandus) in western North America. Patterns of genetic diversity reveal two distinct groups of caribou. Caribou classified as a Northern group, of Beringian origin, exhibited greater number and variability in mtDNA haplotypes compared to a Southern group originating from refugia south of glacial ice. Results indicate that subspecies R. t. granti of Alaska and R. t. groenlandicus of northern Canada do not constitute distinguishable units at mtDNA or microsatellites, belying their current status as separate subspecies. Additionally, the Northern Mountain ecotype of woodland caribou (presently R. t. caribou) has closer kinship to caribou classified as granti or groenlandicus. Comparisons of mtDNA and microsatellite data suggest that behavioural and ecological specialization is a more recently derived life history characteristic. Notably, microsatellite differentiation among Southern herds is significantly greater, most likely as a result of human-induced landscape fragmentation and genetic drift due to smaller population sizes. These results not only provide important insight into the evolutionary history of northern species such as caribou, but also are important indicators for managers evaluating conservation measures for this threatened species.     

Phylogeographical Analysis of mtDNA Data Indicates Postglacial Expansion from Multiple Glacial Refugia in Woodland Caribou (Rangifer tarandus caribou)

Glacial refugia considerably shaped the phylogeographical structure of species and may influence intra-specific morphological, genetic, and adaptive differentiation. However, the impact of the Quaternary ice ages on the phylogeographical structure of North American temperate mammalian species is not well-studied. Here, we surveyed ∼1600 individuals of the widely distributed woodland caribou (Rangifer tarandus caribou) using mtDNA control region sequences to investigate if glacial refugia contributed to the phylogeographical structure in this subspecies. Phylogenetic tree reconstruction, a median-joining network, and mismatch distributions supported postglacial expansions of woodland caribou from three glacial refugia dating back to 13544–22005 years. These three lineages consisted almost exclusively of woodland caribou mtDNA haplotypes, indicating that phylogeographical structure was mainly shaped by postglacial expansions. The putative centres of these lineages are geographically separated; indicating disconnected glacial refugia in the Rocky Mountains, east of the Mississippi, and the Appalachian Mountains. This is in congruence with the fossil record that caribou were distributed in these areas during the Pleistocene. Our results suggest that the last glacial maximum substantially shaped the phylogeographical structure of this large mammalian North American species that will be affected by climatic change. Therefore, the presented results will be essential for future conservation planning in woodland caribou.     

Population structure over a broad spatial scale driven by nonanthropogenic factors in a wide‐ranging migratory mammal,Alaskan caribou

Wide‐ranging mammals face significant conservation threats, and knowledge of the spatial scale of population structure and its drivers is needed to understand processes that maintain diversity in these species. We analysed DNA from 655 Alaskan caribou (Rangifer tarandus granti) from 20 herds that vary in population size, used 19 microsatellite loci to document genetic diversity and differentiation in Alaskan caribou, and examined the extent to which genetic differentiation was associated with hypothesized drivers of population subdivision including landscape features, population size and ecotype. We found that Alaskan caribou are subdivided into two hierarchically structured clusters: one group on the Alaska Peninsula containing discrete herds and one large group on the Mainland lacking differentiation between many herds. Population size, geographic distance, migratory ecotype and the Kvichak River at the nexus of the Alaska Peninsula were associated with genetic differentiation. Contrary to previous hypotheses, small Mainland herds were often differentiated genetically from large interconnected herds nearby, and genetic drift coupled with reduced gene flow may explain this pattern. Our results raise the possibility that behaviour helps to maintain genetic differentiation between some herds of different ecotypes. Alaskan caribou show remarkably high diversity and low differentiation over a broad geographic scale. These results increase information for the conservation of caribou and other migratory mammals threatened by population reductions and landscape barriers and may be broadly applicable to understanding the spatial scale and ecological drivers of population structure in widespread species.     

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.     

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.     

Preliminary studies on the etiology of keratoconjunctivitis in reindeer (Rangifer tarandus tarandus) calves in Alaska

Keratoconjunctivitis outbreaks occur each summer in reindeer (Rangifer tarandus tarandus) herds in western Alaska, USA. This condition has not been well characterized nor has a definitive primary etiologic agent been identified. We evaluated the eyes of 660 calves near Nome, Alaska, between 29 June and 14 July 2005. Clinical signs of keratoconjunctivitis were observed in 26/660 calves (3.9%). Samples were collected from the conjunctival sac of both affected (n=22) and unaffected (n=24) animals for bacterial culture, enzyme-linked immunosorbent assay testing for Chlamydophila psittaci, and for polymerase chain reaction assays for Mycoplasma and Moraxella spp. No primary bacterial or viral etiologic agent(s) were isolated or identified. The cause of keratoconjunctivitis among reindeer calves was not determined, but it could involve an anaerobic bacteria, a difficult-to-isolate viral agent, stress associated with repeated handling, ocular foreign bodies, exposure to corral dust or arthropods, or a combination.     

Plasma urea, creatinine, and urea: creatinine ratio in reindeer (Rangifer tarandus tarandus) and in Svalbard reindeer (Rangifer tarandus platyrhynchus) during defined feeding conditions and in the field.

Variation in plasma urea and creatinine concentration and plasma urea:creatinine ratio (U:C) were studied in semidomestic free-ranging reindeer (Rangifer tarandus tarandus) on the Norwegian mainland, in wild Svalbard reindeer (Rangifer tarandus platyrhynchus), and in captive reindeer maintained either on a lichen-based diet or a protein-rich concentrate to investigate whether these parameters could be used as indicators of the nutritional status of reindeer. In the mainland animals, plasma creatinine concentration was high in winter and early spring and decreased by two-thirds toward the summer. The overall range in mean plasma creatinine concentration (+/-SE) was from 90+/-1.26 to 280+/-2.88 micromol/L. Mean plasma urea concentration (+/-SE) varied from 2.46+/-0.10 in winter up to 17.44+/-0.29 mmol/L in summer and autumn. Month of sampling explained 65% and 90% of the variation in plasma urea and creatinine concentrations, respectively, indicating that seasonality in the diet had the greatest influence on these parameters. Reindeer given lichens as the only feed showed an increase in plasma creatinine and a decrease in plasma urea concentration. Food restriction caused a temporary elevation in urea level but had no significant effect on plasma creatinine concentration. The slight effect of energy intake on urea and creatinine levels was supported by the fact that severe undernutrition in the Svalbard reindeer population had only a small effect on plasma urea and creatinine levels. Protein-rich pellet feed increased plasma urea from around 3 mmol/L to above 10 mmol/L and reduced creatinine concentrations to less than 100 micromol/L, suggesting that the protein content of forage is an important determinant of these blood parameters. Mean U:C ratio (+/-SE) in plasma varied from 8.9+/-0.28 to 120.8+/-1.88. Ratios above 20 appeared when protein intake was low and energy intake was restricted or when protein intake was high. Low ratios occurred when protein intake was low but energy intake adequate. Plasma urea and creatinine concentrations and the U:C ratio showed complex dynamics that were affected by both season and the protein and feed intake. We conclude that they appear to be difficult to interpret as single measures of nutritional status of reindeer.     

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.     

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.     

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.