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Concept: Ovis

167

Sheep scab is an intensively pruritic, exudative and allergic dermatitis of sheep caused by the ectoparasitic mite Psoroptes ovis. The purpose of the present study was to investigate the effect of P. ovis infestation on different components of the ovine epidermal barrier within the first 24 hours post-infestation (hpi). To achieve this, the expression of epidermal differentiation complex (EDC) genes and epidermal barrier proteins, the nature and severity of epidermal pathology and transepidermal water loss (TEWL) were evaluated.By 1 hpi a significant dermal polymorphonuclear infiltrate and a significant increase in TEWL with maximal mean TEWL (598.67 g/m2h) were observed. Epidermal pathology involving intra-epidermal pustulation, loss of epidermal architecture and damage to the basement membrane was seen by 3 hpi. Filaggrin and loricrin protein levels in the stratum corneum declined significantly in the first 24 hpi and qPCR validation confirmed the decrease in expression of the key EDC genes involucrin, filaggrin and loricrin observed by microarray analysis, with 5.8-fold, 4.5-fold and 80-fold decreases, respectively by 24 hpi.The present study has demonstrated that early P. ovis infestation disrupts the ovine epidermal barrier causing significant alterations in the expression of critical barrier components, epidermal pathology, and TEWL. Many of these features have also been documented in human and canine atopic dermatitis suggesting that sheep scab may provide a model for the elucidation of events occurring in the early phases of atopic sensitisation.

Concepts: Protein, Allergy, C-reactive protein, Domestic sheep, Ovis, Sheep, Glossary of sheep husbandry, Sheep husbandry

166

The discovery and identification of Ovis aries (sheep) miRNAs will further promote the study of miRNA functions and gene regulatory mechanisms. To explore the microRNAome (miRNAome) of sheep in depth, samples were collected that included eight developmental stages: the longissimus dorsi muscles of Texel fetuses at 70, 85, 100, 120, and 135 days, and the longissimus dorsi muscles of Ujumqin fetuses at 70, 85, 100, 120, and 135 d, and lambs at 0 (birth), 35, and 70 d. These samples covered all of the representative periods of Ovis aries growth and development throughout gestation (about 150 d) and 70 d after birth. Texel and Ujumqin libraries were separately subjected to Solexa deep sequencing; 35,700,772 raw reads were obtained overall. We used ACGT101-miR v4.2 to analyze the sequence data. Following meticulous comparisons with mammalian mature miRNAs, precursor hairpins (pre-miRNAs), and the latest sheep genome, we substantially extended the Ovis aries miRNAome. The list of pre-miRNAs was extended to 2,319, expressing 2,914 mature miRNAs. Among those, 1,879 were genome mapped to unique miRNAs, representing 2,436 genome locations, and 1,754 pre-miRNAs were mapped to chromosomes. Furthermore, the Ovis aries miRNAome was processed using an elaborate bioinformatic analysis that examined multiple end sequence variation in miRNAs, precursors, chromosomal localizations, species-specific expressions, and conservative properties. Taken together, this study provides the most comprehensive and accurate exploration of the sheep miRNAome, and draws conclusions about numerous characteristics of Ovis aries miRNAs, including miRNAs and isomiRs.

Concepts: DNA, Gene, Chromosome, Harshad number, Longissimus, Domestic sheep, Ovis, Mouflon

28

SUMMARY Ivermectin (IVE), one of the most important anthelmintics, is often used in the treatment of haemonchosis in ruminants. The objective of our work was (1) to find and identify phase I and II metabolites of IVE formed by the Barber’s pole worm (Haemonchus contortus), and (2) to compare IVE metabolites in helminths with IVE biotransformation in sheep (Ovis aries) as host species. Ultrahigh-performance liquid chromatography/tandem mass spectrometry (UHPLC/MS/MS) was used for this purpose. During in vitro incubations, microsomes (from adult worms or from ovine liver) and a primary culture of ovine hepatocytes were incubated with IVE. In the ex vivo study, living H. contortus adults were incubated in the presence of 1 μM IVE for 24 h. The results showed that the H. contortus enzymatic system is not able to metabolize IVE. On the other hand, 7 different phase I as well as 9 phase II IVE metabolites were detected in ovine samples using UHPLC/MS/MS analyses. Most of these metabolites have not been described before. Haemonchus contortus is not able to deactivate IVE through biotransformation; therefore, biotransformation does not contribute to the development of IVE-resistance in the Barber’s pole worm.

Concepts: Metabolism, In vivo, Domestic sheep, Haemonchus contortus, Ovis, Sheep, Mouflon, Barber's pole

28

Pneumonia of bighorn sheep (Ovis canadensis) is a dramatic disease of high morbidity and mortality first described more than 80 years ago. The etiology of the disease has been debated since its initial discovery, and at various times lungworms, Mannheimia haemolytica and other Pasteurellaceae, and Mycoplasma ovipneumoniae have been proposed as primary causal agents. A multi-factorial “respiratory disease complex” has also been proposed as confirmation of causation has eluded investigators. In this paper we review the evidence for each of the candidate primary agents with regard to causal criteria including strength of association, temporality, plausibility, experimental evidence, and analogy. While we find some degree of biological plausibility for all agents and strong experimental evidence for M. haemolytica, we demonstrate that of the alternatives considered, M. ovipneumoniae is the best supported by all criteria and is therefore the most parsimonious explanation for the disease. The strong but somewhat controversial experimental evidence implicating disease transmission from domestic sheep is consistent with this finding. Based on epidemiologic and microbiologic data, we propose that healthy bighorn sheep populations are naïve to M. ovipneumoniae, and that its introduction to susceptible bighorn sheep populations results in epizootic polymicrobial bacterial pneumonia often followed by chronic infection in recovered adults. If this hypothesized model is correct, efforts to control this disease by development or application of vectored vaccines to Pasteurellaceae are unlikely to provide significant benefits, whereas efforts to ensure segregation of healthy bighorn sheep populations from M. ovipneumoniae-infected reservoir hosts are crucial to prevention of new disease epizootics. It may also be possible to develop M. ovipneumoniae vaccines or other management strategies that could reduce the impact of this devastating disease in bighorn sheep.

Concepts: Epidemiology, Bacteria, Causality, Ovis, Mouflon, Bighorn Sheep, Desert Bighorn Sheep, Snow sheep

9

Despite much attention, history of sheep (Ovis aries) evolution, including its dating, demographic trajectory and geographic spread, remain controversial. To address these questions, we generated 45 complete and 875 partial mitogenomic sequences, and performed a meta-analysis of these and published ovine mitochondrial sequences (n = 3,229) across Eurasia. We inferred that O. orientalis and O. musimon share the most recent female ancestor with O. aries at c. 0.790 ma (95% CI: 0.637-0.934 ma) during the Middle Pleistocene, substantially predating the domestication event (c. 8-11 ka). By reconstructing historical variations in effective population size, we found evidence of a rapid population increase c. 20-60 ka, immediately before the Last Glacial Maximum. Analyses of lineage expansions showed two sheep migratory waves at c. 4.5-6.8 ka (lineages A and B: ~6.4-6.8 ka; C: ~4.5 ka) across eastern Eurasia, which could have been influenced by prehistoric West-East commercial trade and deliberate mating of domestic and wild sheep, respectively. A continental-scale examination of lineage diversity and approximate Bayesian computation analyses indicated the Mongolian Plateau region was a secondary center of dispersal, acting as a “transportation hub” in eastern Eurasia: sheep from the Middle Eastern domestication center were inferred to have migrated through the Caucasus and Central Asia, and arrived in North and Southwest China (lineages A, B and C) and the Indian Subcontinent (lineages B and C) via this region. Our results provide new insights into sheep domestication, particularly with respect to origins and migrations to and from eastern Eurasia.

Concepts: Population ecology, Human migration, Indian subcontinent, Asia, Pleistocene, Domestic sheep, Central Asia, Ovis

6

Whole genome sequences (WGS) have proliferated as sequencing technology continues to improve and costs decline. While many WGS of model or domestic organisms have been produced, a growing number of non-model species are also being sequenced. In the absence of a reference, construction of a genome sequence necessitates de novo assembly which may be beyond the ability of many labs due to the large volumes of raw sequence data and extensive bioinformatics required. In contrast, the presence of a reference WGS allows for alignment which is more tractable than assembly. Recent work has highlighted that the reference need not come from the same species, potentially enabling a wide array of species WGS to be constructed using cross-species alignment. Here we report on the creation a draft WGS from a single bighorn sheep (Ovis canadensis) using alignment to the closely related domestic sheep (Ovis aries).

Concepts: DNA, Chromosome, Sequence, Domestic sheep, Ovis, Mouflon, Bighorn Sheep, Snow sheep

5

Ovine psoroptic mange (sheep scab) is a debilitating and damaging condition caused by a hypersensitivity reaction to the faecal material of the parasitic mite Psoroptes ovis. Farmers incur costs from the use of prophylactic acaricides and, if their sheep become infected, they incur the costs of therapeutic treatment plus the economic loss from reduced stock growth, lower reproductive rate, wool loss and hide damage. The unwillingness of farmers to use routine prophylactic treatment has been cited as a primary cause of the growing incidence of sheep scab in the United Kingdom (UK) since the disease was deregulated in 1992. However, if farmers behave rationally from an economic perspective, the optimum strategy that they should adopt will depend on the risk of infection and the relative costs of prophylactic versus therapeutic treatment, plus potential losses. This calculation is also complicated by the fact that the risk of infection is increased if neighbours have scab and reduced if neighbours treat prophylactically. Hence, for any farmer, the risk of infection and optimum approach to treatment is also contingent on the behaviour of neighbours, particularly when common grazing is used. Here, the relative economic costs of different prophylactic treatment strategies are calculated for upland and lowland farmers and a game theory model is used to evaluate the relative costs for a farmer and his/her neighbour under different risk scenarios. The analysis shows that prophylaxis with organophosphate (OP) dipping is a cost effective strategy, but only for upland farmers where the risk of infection is high. In all other circumstances prophylaxis is not cost effective relative to reliance on reactive (therapeutic) treatment. Hence, farmers adopting a reactive treatment policy only, are behaving in an economically rational manner. Prophylaxis and cooperation only become economically rational if the risk of scab infection is considerably higher than the current national average, or the cost of treatment is lower. Should policy makers wish to reduce the national prevalence of scab, economic incentives such as subsidising the cost of acaricides or rigorously applied financial penalties, would be required to make prophylactic treatment economically appealing to individual farmers. However, such options incur their own infrastructure and implementation costs for central government.

Concepts: Immune system, Game theory, Costs, Economics, Policy, Domestic sheep, Ovis, Glossary of sheep husbandry

5

Sheep are thought to have been one of the first livestock to be domesticated in the Near East, thus playing an important role in human history. The current whole mitochondrial genome phylogeny for the genus Ovis is based on: the five main domestic haplogroups occurring among sheep (O. aries), along with molecular data from two wild European mouflons, three urials, and one argali. With the aim to shed some further light on the phylogenetic relationship within this genus, the first complete mitochondrial genome sequence of a Cypriot mouflon (O. gmelini ophion) is here reported. Phylogenetic analyses were performed using a dataset of whole Ovis mitogenomes as well as D-loop sequences. The concatenated sequence of 28 mitochondrial genes of one Cypriot mouflon, and the D-loop sequence of three Cypriot mouflons were compared to sequences obtained from samples representatives of the five domestic sheep haplogroups along with samples of the extant wild and feral sheep. The sample included also individuals from the Mediterranean islands of Sardinia and Corsica hosting remnants of the first wave of domestication that likely went then back to feral life. The divergence time between branches in the phylogenetic tree has been calculated using seven different calibration points by means of Bayesian and Maximum Likelihood inferences. Results suggest that urial (O. vignei) and argali (O. ammon) diverged from domestic sheep about 0.89 and 1.11 million years ago (MYA), respectively; and dates the earliest radiation of domestic sheep common ancestor at around 0.3 MYA. Additionally, our data suggest that the rise of the modern sheep haplogroups happened in the span of time between six and 32 thousand years ago (KYA). A close phylogenetic relationship between the Cypriot and the Anatolian mouflon carrying the X haplotype was detected. The genetic distance between this group and the other ovine haplogroups supports the hypothesis that it may be a new haplogroup never described before. Furthermore, the updated phylogenetic tree presented in this study determines a finer classification of ovine species and may help to classify more accurately new mitogenomes within the established haplogroups so far identified.

Concepts: DNA, Phylogenetics, Computational phylogenetics, Domestic sheep, Ovis, Mouflon, Castlemilk Moorit, Urial

4

Bighorn sheep (Ovis canadensis) were not known to live on Tiburón Island, the largest island in the Gulf of California and Mexico, prior to the surprisingly successful introduction of 20 individuals as a conservation measure in 1975. Today, a stable island population of ∼500 sheep supports limited big game hunting and restocking of depleted areas on the Mexican mainland. We discovered fossil dung morphologically similar to that of bighorn sheep in a dung mat deposit from Mojet Cave, in the mountains of Tiburón Island. To determine the origin of this cave deposit we compared pellet shape to fecal pellets of other large mammals, and extracted DNA to sequence mitochondrial DNA fragments at the 12S ribosomal RNA and control regions. The fossil dung was 14C-dated to 1476-1632 calendar years before present and was confirmed as bighorn sheep by morphological and ancient DNA (aDNA) analysis. 12S sequences closely or exactly matched known bighorn sheep sequences; control region sequences exactly matched a haplotype described in desert bighorn sheep populations in southwest Arizona and southern California and showed subtle differentiation from the extant Tiburón population. Native desert bighorn sheep previously colonized this land-bridge island, most likely during the Pleistocene, when lower sea levels connected Tiburón to the mainland. They were extirpated sometime in the last ∼1500 years, probably due to inherent dynamics of isolated populations, prolonged drought, and (or) human overkill. The reintroduced population is vulnerable to similar extinction risks. The discovery presented here refutes conventional wisdom that bighorn sheep are not native to Tiburón Island, and establishes its recent introduction as an example of unintentional rewilding, defined here as the introduction of a species without knowledge that it was once native and has since gone locally extinct.

Concepts: DNA, Extinction, Ovis, Mouflon, Bighorn Sheep, Desert Bighorn Sheep, Snow sheep, Local extinction

2

The aim of this study was to investigate the presence of β-lactamase producing or fluoroquinolone-resistant members of the family Enterobacteriaceae in European mouflons (Ovis orientalis musimon). The mouflon samples originated from nasal and perineal swabs and/or organ samples in cases of a suspected infection. Only one of the 32 mouflons was tested positive for the presence of Enterobacteriaceae that displayed either an ESBL/AmpC phenotype or were resistant to ciprofloxacin. The positively tested swab originated from a sample of the jejunal mucosa of a four-year old female mouflon. Two different colony morphotypes were identified as Escherichia coli and Klebsiella pneumoniae. These isolates were phenotypically and genotypically characterized in detail by a polyphasic approach. Both isolates were multi-drug resistant. The E. coli isolate belonged to the phylogenetic group B1 and sequence type (ST) 744 and harboured the β-lactamase genes blaCTX-M-15 and blaOXA-1. The K. pneumoniae, identified as ST11, harboured the β-lactamase genes blaSHV-11, blaOXA-1, and blaDHA-1 as well as the plasmid-mediated quinolone resistance (PMQR) gene qnrB55. The present study demonstrates that wild animals can acquire human-derived resistance determinants and such findings may indicate environmental pollution with resistance determinants from other sources.

Concepts: Gene, Evolution, Antibiotic resistance, Escherichia coli, Enterobacteriaceae, Enterobacteria, Ovis, Mouflon