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.     

Foetal Stages of Antler Development

Foetuses of reindeer, Rangifer tarandus tarandus L., were collected at slaughter and studied for structural primordial stages of pedicle formation and antler growth. Fresh foetuses studied in January and February exhibited a round, pale area with an epidermal infolding or groove at the site of the future antler development. Also, in an ethanol-fixed caribou foetus from Alaska, an epidermal invagination could be seen in the area of later pedicle formation. No protruding bone or cartilage was observed as primordial stages of antler growth in reindeer foetuses collected from 10 November to 26 April. It is concluded that an epidermal infolding exists in the foetus of telemetacarpal cervids such as reindeer and caribou.     

Antlers—a Mineral Source in Rangifer

In a calving area on western Hardangervidda, Norway, shed antlers of female reindeer, Rangifer tarandus tarandus L., have been collected for several years. Many of these antlers have been chewed on by reindeer. In the literature antler chewing has been reported to take place on both shed and unshed antlers. Our observations support these findings. Based on the present observations it is suggested that the antlers may subserve the mineral householding of the animals under special conditions. The female reindeer has to pass through a nutritionally marginal season which often coincides with calving. Bringing the bony antlers to the calving areas seems advantageous in the maintenance of calcium balance. The growth of antlers may therefore be looked upon as part of a mineral saving strategy. The mineral stored in the antler thus represents a reserve to be used during pregnancy and lactation. This is in contrast to the common view that shedding of antlers is just waste of mineral when there is a great need for calcium.     

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.     

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.     

Role of oestradiol in the regulation of the seasonal antler cycle in female reindeer, Rangifer tarandus.

Reindeer (or caribou), Rangifer tarandus, is the only extant species of deer in which females as well as males normally develop antlers that are cast and regrown each year. This study investigated the role of ovarian oestradiol in the regulation of the seasonal antler cycle in female reindeer. Ovariectomized Norwegian reindeer living outdoors in northern Norway (69 degrees N) were treated with continuous-release subcutaneous Silastic implants containing oestradiol, which maintained the blood concentrations of oestradiol within the physiological range for the mating season from June to October-November. The treatment with oestradiol induced the synchronized maturation of the antlers and rapid cleaning of the velvet-like skin in August-September in the ovariectomized reindeer, a pattern very similar to that observed in ovary-intact controls living under the same conditions. The removal of the steroid implant in October-November caused the premature casting of the antlers in early winter in two of five animals, while the remainder cast at the normal time in spring; this response was seen whether the animals had received one or two oestradiol implants in autumn. The antlers developed by the ovariectomized, oestradiol-treated females were significantly heavier and carried more branches than the ovariectomized animals without oestradiol replacement, and were marginally heavier than the antlers of intact controls. These results support the view that oestradiol is the biologically active steroid secreted by the ovary in intact female reindeers that induces the normal development of the antlers. Oestradiol stimulates the growth and mineralization of the antler bone, the cleaning of the velvet, and suppresses the casting of the hard antlers. This endocrine control ensures that the hard antlers, which function as weapons, are retained throughout the autumn and winter when the females are normally pregnant and when competition between females over food in the snow is most intense; hence there is a reproductive advantage to explain the evolution of antlers in females.     

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.     

Genetic analyses reveal independent domestication origins of Eurasian reindeer

Although there is little doubt that the domestication of mammals was instrumental for the modernization of human societies, even basic features of the path towards domestication remain largely unresolved for many species. Reindeer are considered to be in the early phase of domestication with wild and domestic herds still coexisting widely across Eurasia. This provides a unique model system for understanding how the early domestication process may have taken place. We analysed mitochondrial sequences and nuclear microsatellites in domestic and wild herds throughout Eurasia to address the origin of reindeer herding and domestication history. Our data demonstrate independent origins of domestic reindeer in Russia and Fennoscandia. This implies that the Saami people of Fennoscandia domesticated their own reindeer independently of the indigenous cultures in western Russia. We also found that augmentation of local reindeer herds by crossing with wild animals has been common. However, some wild reindeer populations have not contributed to the domestic gene pool, suggesting variation in domestication potential among populations. These differences may explain why geographically isolated indigenous groups have been able to make the technological shift from mobile hunting to large-scale reindeer pastoralism independently.     

Interaction of hemoglobin with chloride and 2,3-bisphosphoglycerate. A comparative approach

The equilibrium oxygen-binding properties of hemoglobins from reindeer (Rangifer tarandus tarandus), musk ox (Ovibos muschatos) and a bat (Rousettus aegyptiacus) have been investigated with special reference to the effect of heterotrophic ligands such as chloride and 2,3-bisphosphoglycerate [Gri(2,3)P2]. The results obtained with hemoglobins from reindeer and musk ox indicate that their low oxygen affinity and their insensitivity to Gri(2,3)P2 are not only an intrinsic property of the molecule, as proposed in the case of ruminant hemoglobins, but also the results of the interplay between chloride and Gri(2,3)P2 interactions. In other words, insensitivity of reindeer and musk ox hemoglobins to Gri(2,3)P2 is mainly due to a decreased affinity constant for this cofactor and to an increased affinity constant for chloride anions; this renders more effective the competition of chloride for th anion-binding site. On the other hand bat hemoglobin behaves in a completely different way and could be regarded as a type case of low-affinity hemoglobin since its functional properties are modulated neither by chloride nor by Gri(2,3)P2. The results are discussed in the light of the amino acid residues which are known to be involved in the binding of organic phosphates.     

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.     

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).     

Escaping parasitism in the selfish herd: age, size and density-dependent warble fly infestation in reindeer

It has been suggested that animals may escape attack from mobile parasites by aggregating in selfish herds. A selfish herd disperses the risk of being attacked among its members and the per individual risk of parasite infection should therefore decrease with increasing animal density through the encounter–dilution effect. Moreover, in a selfish herd, dominant and agile animals should occupy the best positions and thereby receive fewer attacks compared to lower ranked animals at the periphery. We tested these predictions on reindeer ( Rangifer tarandus tarandus ) parasitized by warble flies ( Hypoderma tarandi ). Warble flies oviposit their eggs on reindeer during summer and induce strong anti-parasitic behavioural responses in the herds. In this period, reindeer are sexually segregated; females and calves form large and dense herds while males are more solitary. After hatching, the warble fly larvae migrate under the skin of their host where they encyst. In the present study encysted larvae were counted on newly slaughtered hides of male calves and 1.5 year old males from 18 different reindeer herds in Finnmark, northern Norway with large contrasts in reindeer density. In reindeer, body mass is correlated with fitness and social status and we hypothesized that individual carcass mass reflected the animal's ability to occupy the best positions within the herd. Larval abundance was higher among the 1.5 year old males than among the calves. For calves we found in accordance with the selfish herd hypothesis a negative relationship between larval abundance and animal density and between larval abundance and body mass. These relationships were absent for the 1.5 year old males. We suggest that these differences were due to different grouping behaviour where calves and females, but not males, aggregated in selfish herds where they escaped parasitism.     

Arctic life adaptation--I. The function of reindeer hemoglobin

1. The functional properties of hemoglobin from the reindeer (Rangifer tarandus tarandus L.) are characterized as a function of pH, temperature and organic phosphate concentration. 2. Alongside overall similarities shared with most vertebrate hemoglobins, hemoglobin from the reindeer shows significant differences with respect to the effect of both organic phosphates and chloride anions. 3. The limited effect of temperature on oxygen binding (delta H = -4 kcal/mol O2) could be regarded as an interesting case of molecular adaptation to extreme environmental conditions.     

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.     

Novel Rumen Bacterial Diversity in Two Geographically Separated Sub-Species of Reindeer

Svalbard reindeer (Rangifer tarandus platyrhynchus) live under austere nutritional conditions on the high-arctic archipelago of Svalbard, while semi-domesticated Norwegian reindeer (R. tarandus tarandus) migrate between lush coastal summer pastures and inland winter pastures with lichens on mainland Norway. Svalbard reindeer are known to have high rumen concentrations of cellulolytic bacteria, ranging from 15% of the viable population in summer to 35% in winter, compared to only 2.5% in Norwegian reindeer. Their rumen bacterial diversity was investigated through comparative analyses of 16S rRNA gene sequences (∼1.5 kb in length) generated from clone libraries (n = 121) and bacterial isolates (n = 51). LIBSHUFF comparisons of the composition of the two 16S rRNA libraries from Norwegian reindeer showed a significant effect of artificial feeding compared to natural pasture, but failed to yield significant differences between libraries from Norwegian reindeer and Svalbard reindeer. The combined sequences from reindeer were not significantly different from those reported in wild Thompson’s gazelle in Kenya but did differ from those reported in domestic cattle in Japan. A total of 90 distinct operational taxonomic units (OTUs) were identified by employing a criterion of 97% similarity, while the Chao1 index estimated the reindeer bacterial rumen population richness at 698 OTUs. The majority of the clone library sequences (92.5%) represented novel strains with <97% identity to any known sequence in the public database, most of them affiliated with the bacterial phylum Firmicutes (low G+C Gram-positives) related to the order Clostridiales (76.7%), while Gram-negative bacteria in the Bacteriodales (Prevotella–Bacteroides group) contributed to 22.5%. Also, six of the isolates were putatively novel strains, possibly representing new species in the Clostridium subphylum (cluster XIVa), Actinomyces and Butyrivibrio.     

Diet shift of a facultative scavenger, the wolverine, following recolonization of wolves

1. Wolves Canis lupus L. recolonized the boreal forests in the southern part of the Scandinavian peninsula during the late 1990s, but so far there has been little attention to its effect on ecosystem functioning. Wolf predation increases the availability of carcasses of large prey, especially moose Alces alces L., which may lead in turn to a diet switch in facultative scavengers such as the wolverine Gulo gulo L. 2. Using 459 wolverine scats collected during winter-spring 2001-04 for DNA identity and dietary contents, we compared diet inside and outside wolf territories while controlling for potential confounding factors, such as prey density. We tested the hypothesis that wolverine diet shifted towards moose in the presence of wolves, while taking into account possible sexual segregation between the sexes. Occurrence of reindeer, moose and small prey was modelled against explanatory covariates using logistic mixed-effects models. Furthermore, we compared diet composition and breadth among habitats and sexes. 3. Occurrence of reindeer, moose and small prey in the diet varied with prey availability and habitat. As expected, diet contained more moose and less reindeer and small prey in the presence of wolves. Their diet in tundra consisted of 40% reindeer Rangifer tarandus L., 39% moose and 9% rodents. In forest with wolf, their diet shifted to 76% moose, 18% reindeer and 5% rodents; compared to 42% moose, 32% reindeer and 15% rodents in forest without wolf. This diet switch could not be explained by higher moose density in wolf territories. Female diet consisted of more small prey than for males, but there was a tendency for females to use the highly available moose carrion opportunistically and to hunt less on small prey within wolf territories. 4. Our study highlights how wolves increase scavenging opportunities for wolverines, and how sexual differences in diet may also apply to large scavengers. Due to their more restricted home range, female wolverines are forced to rely more on hunting small prey. The relatively high occurrence of wolf kills, however, forms an important food source to wolverines in this area. The recolonization of wolves may therefore have contributed to the consequent recolonization of wolverines into the same area.     

Glucuronidation in the reindeer: dietary modification in the UDP-glucuronosyltransferase activity with 4-nitrophenol, 1-naphthol and phenolphthalein as acceptors

The UDP-glucuronosyltransferase activity towards 4-nitrophenol, 1-naphthol and phenolphthalein was measured from the hepatic microsomes of the reindeer (Rangifer tarandus tarandus) after summer, autumn and winter feeding periods. The microsomes were digested with trypsin or digitonin. The UDP-glucuronosyltransferase activity with 4-nitrophenol and 1-naphthol as aglycones was lower in reindeer on winter food than in ones on summer food after trypsin and digitonin digestion. The activity towards phenolphthalein was the same in each feeding period. The different seasonal feeding affects the structure of microsomal membranes and this is reflected as modifications of the UDP-glucuronosyltransferase towards different substrates.     

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.     

Age-related changes in the testicular and antler cycles of reindeer, Rangifer tarandus

A total of 111 male reindeer of various ages was shot in all months of the year to study the relationship between the seasonal changes in testicular activity and the antler cycle. From the changes in testis weight, seminiferous tubular tissue area and plasma testosterone values and the occurrence of spermatogenesis, it is concluded that calves attain physiological puberty in their first year, during which they also complete an antler cycle. The amplitude of the cyclical change in testis weight and plasma testosterone values increases with age and can be correlated with the earlier onset of events in the spermatogenic and antler cycles of older animals. The duration of the spermatogenic and testosterone cycles of reindeer is short, and is inversely related to the long period spent without antlers. It is suggested that testosterone strongly influences the antler cycle of reindeer males.     

Strain rate dependence of the mechanical properties of reindeer antler and the cumulative damage model of bone fracture

Carter and Caler have produced a 'cumulative damage' model for the fracture of bone, based on creep experiments on human bone, which has been corroborated by monotonic tensile tests on bone, loaded at various strain rates. Monotonic tensile tests on reindeer's antler, which has a lower modulus of elasticity than human bone, produce very similar results. Unlike human bone, reindeer antler always shows a large post-yield strain, and it is possible to distinguish pre-yield and post-yield behaviour. The 'final stiffness' (ultimate stress/ultimate strain) is invariant with strain rate. This is confirmation that bone fractures when a certain amount of damage has accumulated. However, reindeer antler shows a considerable post-yield increase in stress. This is difficult to accommodate in a cumulative damage model.