Genetic diversity of Nubian ibex in comparison to other ibex and domesticated goat species

Capra nubiana is a wild ibex species that is in danger of extinction. This study aimed at assessing the genetic diversity and population structure of Nubian ibex (Capra nubiana, n?=?8) in comparison to Alpine ibex (Capra ibex, n?=?8), Bezoar ibex (Capra aegagrus, n?=?4), and domesticated Taggar goats (Capra aegagrus hircus, n?=?24). All animals were genotyped with the 50K goat SNP chip. Since commercial SNP chips are not designed for wild species, data analysis was done in two ways: (1) using all callable SNPs (33,698) and (2) with a reduced set of SNPs segregating within three out of four populations (662). Using these two sets of SNPs, the observed heterozygosity in Nubian ibex ranged from 0.02 to 0.44, in Alpine ibex from 0.01 to 0.38, and in Bezoar ibex from 0.13 to 0.38, when analyzing 33,698 or 662 SNPs, respectively. In domesticated Taggar goats, the values for the observed heterozygosity using all 33,698 callable SNPs and the reduced set of 662 SNPs were similar (0.40–0.41). Pairwise F_ST values for the differentiation between species ranged from 0.17–0.35 (Bezoar ibex vs. Taggar goats) to 0.47–0.91 (Bezoar vs. Alpine ibex), and was 0.33–0.90 between Bezoar and Nubian ibex, respectively, to the two sets of SNPs. The analysis of molecular variance among all animals revealed that 74–78% can be explained by differences between species, while the residual 22–26% result from differences among individuals, respectively. Cluster analysis of Nei’s genetic distance allowed to detected two distinct clusters comprising Nubian and Alpine ibex on one hand and Taggar goats and Bezoar ibex on the other hand, and clear separation of all four breeds. Principal component (PC) analysis confirmed and further refined the clusters. SNPs that contributed most to PC1 allowed us to identify genomic regions accounting for the distances between species. These regions contain known milk protein genes. The identification of milk protein genes as contributors to the differentiation between species provides insights into the domestication of wild Capra breeds.     

Some coccidia from the Nubian ibex (Capra ibex Nubiana Cuvier, 1825)

The authors describe three coccidian species (eimeria arloingi, E. ninakohylakimovae, E. parva) found in the faeces of some Nubian ibexes (Capra ibex nubiana) in the "Hai-Bar Wildlife Reserve", Israel. The results of the study represent the first finding of coccidia in C. ibex nubiana.     

Group dynamics of the Nubian ibex (Capra ibex nubiana) in the Tuwayiq Canyons, Saudi Arabia

Group dynamics of the Nubian ibex ( Capra ibex nubiana ), a sub-species adapted to arid environments, were studied at the Ibex Reserve, Saudi Arabia. Most of the animals (83%) were seen in mixed herds during the rut and post-rut. Mean group size of all sex-age categories was 7.2, with the majority of the ibex seen in groups of < 10. The sex ratio of adult animals was equal but that of juveniles, older than six months, was skewed towards females. Habitat structure, sparse vegetation cover and a small population size are factors that favour small group size. An equal adult sex ratio and a high number of juveniles indicate that the population has a high reproductive potential.     

Introgression from Domestic Goat Generated Variation at the Major Histocompatibility Complex of Alpine Ibex

The major histocompatibility complex (MHC) is a crucial component of the vertebrate immune system and shows extremely high levels of genetic polymorphism. The extraordinary genetic variation is thought to be ancient polymorphisms maintained by balancing selection. However, introgression from related species was recently proposed as an additional mechanism. Here we provide evidence for introgression at the MHC in Alpine ibex (Capra ibex ibex). At a usually very polymorphic MHC exon involved in pathogen recognition (DRB exon 2), Alpine ibex carried only two alleles. We found that one of these DRB alleles is identical to a DRB allele of domestic goats (Capra aegagrus hircus). We sequenced 2489 bp of the coding and non-coding regions of the DRB gene and found that Alpine ibex homozygous for the goat-type DRB exon 2 allele showed nearly identical sequences (99.8%) to a breed of domestic goats. Using Sanger and RAD sequencing, microsatellite and SNP chip data, we show that the chromosomal region containing the goat-type DRB allele has a signature of recent introgression in Alpine ibex. A region of approximately 750 kb including the DRB locus showed high rates of heterozygosity in individuals carrying one copy of the goat-type DRB allele. These individuals shared SNP alleles both with domestic goats and other Alpine ibex. In a survey of four Alpine ibex populations, we found that the region surrounding the DRB allele shows strong linkage disequilibria, strong sequence clustering and low diversity among haplotypes carrying the goat-type allele. Introgression at the MHC is likely adaptive and introgression critically increased MHC DRB diversity in the genetically impoverished Alpine ibex. Our finding contradicts the long-standing view that genetic variability at the MHC is solely a consequence of ancient trans-species polymorphism. Introgression is likely an underappreciated source of genetic diversity at the MHC and other loci under balancing selection.     

Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes

Maintaining genetic variation and minimizing inbreeding are central goals of conservation genetics. It is therefore crucial to understand the important population parameters that affect inbreeding, particularly in reintroduction programs. Using data from 41 reintroduced Alpine ibex (Capra ibex ibex) populations we estimated inbreeding since the beginning of reintroductions using population-specific Fst, and inbreeding over the last few generations with contemporary effective population sizes. Total levels of inbreeding since reintroduction of ibex were, on average, close to that from one generation of half-sib mating. Contemporary effective population sizes did not reflect total inbreeding since reintroduction, but 16% of variation in contemporary effective population sizes among populations was due to variation in current population sizes. Substantial variation in inbreeding levels among populations was explained by founder group sizes and the harmonic mean population sizes since founding. This study emphasizes that, in addition to founder group sizes, early population growth rates are important parameters determining inbreeding levels in reintroduced populations.     

Techniques for noninvasive genetic monitoring of Alpine Ibex <Emphasis Type="Italic">Capra ibex</Emphasis>

Noninvasive sampling is of increasing importance for the molecular genetic monitoring of wild animal populations, although reduced quality and quantity of such samples’ DNA can affect genetic data and their subsequent interpretation. Consequently, we performed a pilot study to establish a feasible approach for the genetic investigation of free-ranging Alpine ibex Capra ibex Linnaeus, 1758 populations. Establishing an ibex-specific PCR-RFLP based on Cytochrome b gene differences allowed the discrimination of noninvasive ibex samples from those of other sympatric ungulates. In addition, we established a quantitative PCR for ibex samples. The quantification of 35 faecal samples clearly exhibited a strong variability of DNA contents among samples and individuals. Furthermore, we performed threefold genotyping experiments on six microsatellite loci to determine the extent of genotyping errors in reference to blood samples of the respective individuals. The analyses exhibited a strong dependence of erroneous microsatellite genotypes on the starting amount of template DNA. Variability in reliability was observed between individual loci, resulting in a mandatory high DNA concentration necessary for consistent genotyping. This study serves as basis for further ibex research and we propose the application of DNA quantification of faecal samples to focus genotyping efforts solely on suitable samples.     

Tear production in three captive wild herbivores in Israel

The Schirmer tear test (STT) I was performed to evaluate tear production in 12 captive Nubian ibex (Capra ibex nubiana), 10 captive Burchell's zebras (Equus burchelli) and five Arabian oryx (Oryx leucoryx) at the Tel-Aviv Ramat-Gan Zoological Center (Israel). Mean (+/- standard deviation) STT values were 13.2 +/- 5.1 mm/min in the ibex, 23.4 +/- 3.4 mm/min in the zebra and 12.7 +/- 4.8 mm/min in the oryx. There were no significant effects of gender, age, weight, or side of the eye. There were no significant differences in STT values between ibex and oryx, but tear production in both species was significantly lower than in zebras. Knowledge of normal tear production values is important for the differential diagnosis of conjunctivitis and keratitis in these species.     

Effects of climate on population fluctuations of ibex

Predicting the effects of the expected changes in climate on the dynamics of populations require that critical periods for climate‐induced changes in population size are identified. Based on time series analyses of 26 Swiss ibex (Capra ibex) populations, we show that variation in winter climate affected the annual changes in population size of most of the populations after accounting for the effects of density dependence and demographic stochasticity. In addition, precipitation during early summer also influenced the population fluctuations. This suggests that the major influences of climate on ibex population dynamics operated either through loss of individuals during winter or early summer, or through an effect on fecundity. However, spatial covariation in these climate variables was not able to synchronize the population fluctuations of ibex over larger distances, probably due to large spatial heterogeneity in the effects of single climate variables on different populations. Such spatial variation in the influence of the same climate variable on the local population dynamics suggests that predictions of influences of climate change need to account for local differences in population dynamical responses to climatic conditions.     

Steinbock und Gemse im Alpenraum – genetische Variabilität und biochemische Differenzierung zwischen den Arten

Ibex and chamois of the Alps – genetic variability and biochemical differentiation between species Genetic variability of 46 specimens of ibex (Capra ibex ibexL.) from Graubünden/Switzerland was investigated by means of horizontal starch gel electrophoresis. Twenty four isoenzyme systems were examined in kidney and liver tissues. From 38 loci scored 5.3 % were polymorphic (PGM-2, ADA-1) and average heterozygosity was 0.0235. The comparatively low proportion of polymorphic loci can be interpreted as the result of a bottleneck in alpine ibex during the last centuries. Based on a ¯-value of 0,2746 a time of divergence between ibex and chamois of about 1370000 years was calculated.     

Sexual differences in the behavioural response to a variation in predation risk

Predators may influence their prey populations not only through direct lethal effects, but also by causing behavioural changes. The natural expansion of the wolf (Canis lupus) into the Alps provided the rare opportunity to monitor the responses of a prey species to the return of a large predator. Density effects have rarely been considered in the study of antipredator strategies. We examined the effects of wolf recolonisation and density modifications on group size and use of safe areas by Alpine ibex (Capra ibex) in Gran Paradiso National Park (Italy), where no large terrestrial predator has been present for about a century. We documented that, in a few years, the variation in the factors affecting the landscape of fear caused significant modifications in ibex behavioural patterns that could not be accounted for by density changes only. Male groups decreased in size and moved closer to safer areas. The distance of female groups from refuge sites, instead, was not affected, and their propensity to live in groups was scarcely modified. Behavioural modifications likely caused a reduction in nutrient intake in adult male ibex, as they necessarily used lower‐quality feeding patches. Our results showed that male and female ibex, which are characterised by a strong dimorphism, adopted different strategies to solve the conflicting demands of foraging efficiently and avoiding predators.     

Effects of food quality, diet preference and water on patch use by Nubian ibex

Measuring patch use of a forager can reveal not only its cost and benefits from foraging, but also the importance of environmental factors and the significance of energy, nutrients and predation risk to its fitness. In order to assess the effects of various variables that may affect the foraging behavior of free-ranging Nubian ibex in the Negev Desert, Israel, giving-up densities (GUD) in artificial food patches were measured following Kotler et al. In particular, we tested the effects of food quality and water availability on Nubian ibex foraging behavior. To do so, we (1) tested whether the tannic acid content of food affected diet preferences, (2) assayed their diet selection strategy, (3) tested if the foraging decisions of the Nubian ibex were affected by the availability of water and (4) determined the nutritional relationship between food resources and water. Nubian ibex had lower GUDs and used resources patches more intensively where water was available, the food quality was higher and the location was closer to the escape terrain. Nubian ibex showed an expanding specialist diet selection when exploiting resource patches with a mix of items that differ in quality. Overall, food and water were complementary resources for Nubian ibex, and tannins reduced food quality. These factors help to determine patch foraging behavior decisions in Nubian ibex and contribute to habitat quality.     

Dynamic social system in Nubian ibex: can a second mating season develop in response to arid climate?

We studied a population of Nubian ibex Capra ibex nubiana in the eastern extreme of its range, the hyper-arid central desert of the Sultanate of Oman. Long-term data were collected from January 1983 to December 1997 by direct observation, as well as VHF telemetry on 12 animals (eight from 1987 to 1990; four from 1994 to 1996). We recorded 884 sightings: 40.4% of single animals and 59.6% of groups. Although no significant monthly variation of group size (Jarman's Typical Group Size) was found, there were distinct peaks in March (4.0 ind. group⁻¹) and September (5.1 ind. group⁻¹). Groups of males and females formed especially in March and November, and female–kid groups in February and July–August. Our data may suggest two mating periods: the first one in autumn (similar to the rut of ibex in temperate mountain areas), with kids born in spring/early summer, after winter–spring rainfall, and the second one in spring, with kids born in late summer/autumn, before winter–spring rainfalls. We suggest that the second rutting period may have evolved as a micro-evolutionary process, with the local population adapting to hyper-arid environment constraints. The spring mating season may favour only females in prime conditions, who can afford a pregnancy in the local severe summers and will deliver kids when plant greening begins, in the autumn, whereas the autumn (original) mating season may be afforded by any female, but kids will be born in an unfavourable period, before the summer drought.     

Cohabitation of a <Emphasis Type="Italic">Brucella melitensis</Emphasis> infected Alpine ibex (<Emphasis Type="Italic">Capra ibex</Emphasis>) with domestic small ruminants in an enclosure in Gran Paradiso National Park,in Western Italian Alps

After the first report of Brucella melitensis infection from a 7-year-old alpine ibex (Capra ibex) buck living in Gran Paradiso National Park (GPNP), further studies demonstrated the presence of the infection in ibex and chamois. Considering that livestock herds keep on sharing pastures with more than 3,500 ibex and 9,000 chamois in the park, our aim was to demonstrate under controlled conditions the possibility of Brucella infection passing from wild ruminants to livestock. A 7-year-old male alpine ibex with clinical signs of brucellosis and serologically positive was released in a 5,000 m² enclosure together with five goats and two sheep rams. Due to poor condition, ibex was suppressed at day 40, domestic ruminants stayed into the enclosure potentially contaminated by ibex for further 38 days. During this period, we had monitored our animals taking blood from domestic ruminants every 15 days and tested the serum to Rose Bengal agglutination test and Complement Fixation test. Domestic animals tested negative at serology at all sampling time and at isolation, while B. melitensis biovar 3 was isolated from ibex tissues. Our data show that transmission of infection from ibex to livestock is not easy. After 40 days of strict cohabitation and 38 days of permanence in an area where an infected ibex lives, no one of the domestic animals contracted infection. In spite of the limitation of our field trial, we have demonstrated that long direct and indirect contact between alpine ibex and domestic animals will not easily lead to an infection of the latter. Further investigations are needed to confirm our results and evaluate the effective risk of B. melitensis transmission from alpine ibex to livestock.     

Nitrogen metabolism and kidney function in the Nubian ibex (Capra ibex nubiana)

The nitrogen economy of the Nubian ibex (Capra ibex nubiana), a ruminant that inhabits harsh deserts, was studied in the laboratory when fed three diets of different quality. Even on the low quality roughage (wheat straw) the ibex was found capable of balancing its nitrogen economy. On feeds low in protein, recycling of urea played a major role in helping the ibex maintaining a balanced nitrogen metabolism. When on wheat straw, the ibex recycled 71.6% of the urea synthesized in its liver. When on feeds lower in protein, blood urea concentration dropped (from 11.4 mM when on alfalfa hay to 3.2 mM when on wheat straw). GFR that amounted to 44.28 ml/min when on alfalfa hay decreased to 28.97 ml/min when on wheat straw. Reabsorption of urea amounted to 48% of the urea filtered when on alfalfa hay and increased to 78.8% on wheat straw.     

A robust sequencing assay of a thousand amplicons for the high-throughput population monitoring of Alpine ibex immunogenetics

Polymorphism for immune functions can explain significant variation in health and reproductive success within species. Drastic loss in genetic diversity at such loci constitutes an extinction risk and should be monitored in species of conservation concern. However, effective implementations of genome-wide immune polymorphism sets into high-throughput genotyping assays are scarce. Here, we report the design and validation of a microfluidics-based amplicon sequencing assay to comprehensively capture genetic variation in Alpine ibex (Capra ibex). This species represents one of the most successful large mammal restorations recovering from a severely depressed census size and a massive loss in diversity at the major histocompatibility complex (MHC). We analysed 65 whole-genome sequencing sets of the Alpine ibex and related species to select the most representative markers and to prevent primer binding failures. In total, we designed ~1,000 amplicons densely covering the MHC, further immunity-related genes as well as randomly selected genome-wide markers for the assessment of neutral population structure. Our analysis of 158 individuals shows that the genome-wide markers perform equally well at resolving population structure as RAD-sequencing or low-coverage genome sequencing data sets. Immunity-related loci show unexpectedly high degrees of genetic differentiation within the species. Such information can now be used to define highly targeted individual translocations. Our design strategy can be realistically implemented into genetic surveys of a large range of species. In conclusion, leveraging whole-genome sequencing data sets to design targeted amplicon assays allows the simultaneous monitoring of multiple genetic risk factors and can be translated into species conservation recommendations.     

Habitat selection in translocated gregarious ungulate species: An interplay between sociality and ecological requirements

The adaptation of translocated organisms to a new environment in the first years after their release is crucial in translocation programs because it may affect survival and reproductive success. Therefore, identifying the factors determining resource selection by the relocated animals is essential to improve the planning and the outcome of such programs. Using data collected in 2006–2009 in the framework of a restocking program, we studied the temporal variation of habitat selection in 14 translocated Alpine ibex (Capra ibex) during the year of their release and the following 3 years. We hypothesized a progressive adaptation of the translocated individuals, highlighted by a gradual decrease in the dissimilarities between translocated and resident individuals in ecological characteristics and social behavior. We tested the differences in habitat selection and home range size between the translocated and resident individuals and compared the spatial overlap between the groups. As expected, the dissimilarities decreased annually. The translocated and resident ibex almost immediately selected the same habitat resources, but the translocated individuals required 3 years to become fully socially assimilated. Our results indicated that habitat selection by gregarious species in a new environment is primarily driven by specific ecological requirements and that sociality plays a significant role. The translocated individuals tended to colonize areas already occupied by residents, either to fulfill social requirements and/or because the location of resident individuals may indicate high-quality habitat. This pattern of behavior must be considered in the planning of translocation programs because habitat selection can affect the outcomes of the programs. © 2013 The Wildlife Society.     

Microsatellite-based genotyping of MHC class II DRB1 gene in Iberian and Alpine ibex

In an analysis of a microsatellite locus (OLADRB1) linked to the MHC DRB1 gene of Iberian and Alpine ibex (Capra pyrenaica and Carpa ibex), we detected strong linkage disequilibrium between both loci. The allele length polymorphism at OLADRB1 was unambiguously linked to a particular DRB1 allele. This allowed us to develop a DRB-STR matching method for both ibex species. Validation of the DRB-STR matching method was performed in 160 Iberian ibex from Spain and 98 Alpine ibex from Switzerland and Italy. This simple and relatively inexpensive protocol may find wide applications in a variety of research areas (e.g., mate choice, pathogen-driven selection) and in the biological conservation and management of the Western European ibex populations.     

Evidence for African origins of founders of the asiatic lion species survival plan

The Asiatic lion (Panthera leo persica) exists in the wild as a single relict population of approximately 250 individuals in the protected Gir Forest Sanctuary in western India. In 1981, a species survival plan (SSP) for the Asiatic lion was established by the American Association of Zoological Parks and Aquariums to manage the 200 + descendants of Asiatic lions in captivity in western zoological facilities. This captive population was derived from seven founders. In order to compare the genetic structure of the Gir Forest population with that of the captive SSP population, a genetic survey of 46 electrophoretic allozyme systems resolved from extracts of lion blood was undertaken by using 29 SSP Asiatic lions and 28 wild-caught or captive-bred lions maintained at the Sakkarbaug Zoo in India but originally derived from the Gir Forest. The Gir lion population was found to be genetically monomorphic at each of 46 allozyme loci. This was in contrast to several African lion (Panthera leo leo) populations, which show moderate levels of allozyme variation at the same loci. The SSP lion population was polymorphic at three allozyme loci (IDHI, TF, and PTI) for alleles that were previously found only in African lion populations. Pedigree analysis of the genetic transmission of these three biochemical loci demonstrated that two of the five primary founder animals of the SSP Asiatic lion population (a breeding pair originally imported from the Trivandrum Zoo in southern India) were descendants of the African subspecies. Three other founder animals were pure Asian. A retrospective SSP pedigree analysis of two morphologic characters (prominent abdominal fold and pairing of infraorbital foramen) that are partially diagnostic for persica vs leo was consistent with this conclusion as well. The implications for the management of small captive populations of threatened species and of the Asiatic lion SSP population are discussed.     

To Feed or Not to Feed? Testing Different Hypotheses on Rut‐Induced Hypophagia in a Mountain Ungulate

In many ruminant species, males dramatically reduce forage intake during the rut. To date, different hypotheses have been suggested to explain this rut‐induced hypophagia. To assess the predictions of the main hypotheses, we analysed Alpine ibex (Capra ibex) activity budget and compared the behaviour of males and females before, during, and after the rut. Only males spent significantly less time foraging during the rut than outside of it, whereas females allocated a similar proportion of time to foraging before, during, and after the rut. Our results showed that during the rut males also reduced lying time, while the ratio of time spent feeding to time spent lying did not change for males among periods. In conclusion, during the breeding season males maximized energy intake when not actively engaged in mating activities and rut‐induced hypophagia appeared to result from time budget constraints generated by mating‐related activities. Accordingly, the foraging constraint hypothesis seems appropriate to explain this phenomenon in Alpine ibex males.     

Nutritional ecology of dimorphic herbivores: digestion and passage rates in Nubian ibex

We compared forage digestion and passage rates among three groups of Nubian ibex (Capra ibex nubiana) — mature males, non-lactating females, and lactating females — to test hypotheses relating intraspecific digestive ability to body mass and reproduction costs. We hypothesized that large males (60 kg) would exhibit longer forage retention times and more complete digestion of fermentable cell walls than adult females (23 kg). We tested these predictions by measuring digestion and retention of a grass hay and an alfalfa hay, forages that exhibited contrasting rates and extents of cell wall digestion. Consistent with predictions, males retained both forages longer than non-lactating females. However, by substantially increasing gut fill, lactating females increased both intake and retention time with respect to non-lactating females. Contrary to predictions, all three groups digested the grass (66% digestible) and alfalfa hay (63%) equally well. Alfalfa cell wall was less digestible than that of grass hay (60% vs 69% digestible), and retention time of alfalfa was consistently, but not statistically significantly, shorter. Fiber digestion was not correlated with retention time, emphasizing the ability of behavioral processes to modify digestion rate. We postulate that females achieved their greater digestion rate by masticating forages much more thoroughly than males.