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Concept: Przewalski's Horse

176

An equine SNP genotyping array was developed and evaluated on a panel of samples representing 14 domestic horse breeds and 18 evolutionarily related species. More than 54,000 polymorphic SNPs provided an average inter-SNP spacing of ∼43 kb. The mean minor allele frequency across domestic horse breeds was 0.23, and the number of polymorphic SNPs within breeds ranged from 43,287 to 52,085. Genome-wide linkage disequilibrium (LD) in most breeds declined rapidly over the first 50-100 kb and reached background levels within 1-2 Mb. The extent of LD and the level of inbreeding were highest in the Thoroughbred and lowest in the Mongolian and Quarter Horse. Multidimensional scaling (MDS) analyses demonstrated the tight grouping of individuals within most breeds, close proximity of related breeds, and less tight grouping in admixed breeds. The close relationship between the Przewalski’s Horse and the domestic horse was demonstrated by pair-wise genetic distance and MDS. Genotyping of other Perissodactyla (zebras, asses, tapirs, and rhinoceros) was variably successful, with call rates and the number of polymorphic loci varying across taxa. Parsimony analysis placed the modern horse as sister taxa to Equus przewalski. The utility of the SNP array in genome-wide association was confirmed by mapping the known recessive chestnut coat color locus (MC1R) and defining a conserved haplotype of ∼750 kb across all breeds. These results demonstrate the high quality of this SNP genotyping resource, its usefulness in diverse genome analyses of the horse, and potential use in related species.

Concepts: Genetics, Horse, Population genetics, Rhinoceros, Odd-toed ungulate, Equus, Przewalski's Horse, Tarpan

34

The rich fossil record of equids has made them a model for evolutionary processes. Here we present a 1.12-times coverage draft genome from a horse bone recovered from permafrost dated to approximately 560-780 thousand years before present (kyr bp). Our data represent the oldest full genome sequence determined so far by almost an order of magnitude. For comparison, we sequenced the genome of a Late Pleistocene horse (43 kyr bp), and modern genomes of five domestic horse breeds (Equus ferus caballus), a Przewalski’s horse (E. f. przewalskii) and a donkey (E. asinus). Our analyses suggest that the Equus lineage giving rise to all contemporary horses, zebras and donkeys originated 4.0-4.5 million years before present (Myr bp), twice the conventionally accepted time to the most recent common ancestor of the genus Equus. We also find that horse population size fluctuated multiple times over the past 2 Myr, particularly during periods of severe climatic changes. We estimate that the Przewalski’s and domestic horse populations diverged 38-72 kyr bp, and find no evidence of recent admixture between the domestic horse breeds and the Przewalski’s horse investigated. This supports the contention that Przewalski’s horses represent the last surviving wild horse population. We find similar levels of genetic variation among Przewalski’s and domestic populations, indicating that the former are genetically viable and worthy of conservation efforts. We also find evidence for continuous selection on the immune system and olfaction throughout horse evolution. Finally, we identify 29 genomic regions among horse breeds that deviate from neutrality and show low levels of genetic variation compared to the Przewalski’s horse. Such regions could correspond to loci selected early during domestication.

Concepts: Evolution, Horse, Wild horse, Equus, Equidae, Donkey, Domestication of the horse, Przewalski's Horse

26

The maintenance and development of conservation areas by grazing of large herbivores, such as Przewalski’s horses, is common practice. Several nature conservation areas house male bachelor groups of this species. When males are needed for breeding they are removed from the groups, often without considering group compositions and individual social positions. However, alpha animals are needed for ensuring group stability and decision making in potentially dangerous situations in several species. To investigate the role of the alpha male in a bachelor group, we observed the behaviour of five Przewalski’s horse males during the enlargement of their enclosure. We analyzed the group’s social structure and movement orders, as well as the animals' connectedness, activity budgets, and whether they moved with preferred group members and how factors such as social rank influenced the horses' behaviour. We also investigated the excretion of glucocorticoid metabolites (GCM) via faeces of the horses while exploring a new area as a parameter of glucocorticoid production. Our results show that the alpha male is important for a bachelor group in changing environmental conditions. The alpha male had the highest level of connectedness within the group. When exploring the new environment, its position in the group changed from previously being the last to being the first. Furthermore the whole group behaviour changed when exploring the new area. The stallions showed reduced resting behavior, increased feeding and did not stay close to each other. We found that the excretion of glucocorticoid metabolites of most horses rose only marginally during the first days on the new area while only the alpha male showed a significant increased amount of glucocorticoid production during the first day of the enclosure enlargement.

Concepts: Psychology, Insect, Sociology, Horse, Human behavior, Social relation, Conservation, Przewalski's Horse

25

The Przewalski’s horse (Equus ferus przewalskii), the only remaining wild horse within the equid family, is one of only a handful of species worldwide that went extinct in the wild, was saved by captive breeding, and has been successfully returned to the wild. However, concerns remain that after multiple generations in captivity the ecology of the Przewalski’s horse and / or the ecological conditions in its former range have changed in a way compromising the species' long term survival. We analyzed stable isotope chronologies from tail hair of pre-extinction and reintroduced Przewalski’s horses from the Dzungarian Gobi and detected a clear difference in the isotopic dietary composition. The direction of the dietary shift from being a mixed feeder in winter and a grazer in summer in the past, to a year-round grazer nowadays, is best explained by a release from human hunting pressure. A changed, positive societal attitude towards the species allows reintroduced Przewalski’s horses to utilize the scarce, grass-dominated pastures of the Gobi alongside local people and their livestock whereas their historic conspecifics were forced into less productive habitats dominated by browse.

Concepts: Horse, Livestock, Wild horse, Equus, Przewalski's Horse, Tarpan, Mustang

23

‘The invisible horse’ was the central topic discussed at a conference organised by the equine charity World Horse Welfare in London last month. Gill Harris reports.

Concepts: Horse, Equus, Equidae, Donkey, Pony, Przewalski's Horse, Tarpan, Onager

10

1. Competition among sympatric wild herbivores is reduced by different physiological, morphological, and behavioral traits resulting in different dietary niches. Wild equids are a rather uniform group of large herbivores which have dramatically declined in numbers and range. Correlative evidence suggests that pasture competition with livestock is one of the key factors for this decline, and the situation may be aggravated in areas where different equid species overlap. 2. The Dzungarian Gobi is currently the only place where two wild equid species coexist and share the range with the domesticated form of a third equid species. In the arid and winter cold Gobi, pasture productivity is low, highly seasonal, and wild equids additionally face increasing livestock densities. 3. We used stable isotope chronologies of tail hairs to draw inferences about multi-year diet seasonality, isotopic dietary niches, and physiological adaptations in the Asiatic wild ass (khulan), reintroduced Przewalski’s horse, and domestic horse in the Mongolian part of the Dzungarian Gobi. 4. Our results showed that even in the arid Gobi, both horse species are predominantly grazers, whereas khulan are highly seasonal, switching from being grazers in summer to mixed feeders in winter. The isotopic dietary niches of the two horse species were almost identical, did not vary with season as in khulan, and were narrower than in the latter. Higher δ(15)N values point towards higher water use efficiency in khulan, which may be one reason why they can exploit pastures further away from water. 5. Synthesis and applications: The high degree of isotopic dietary niche overlap in the two horses points towards a high potential for pasture competition during the critical nutritional bottleneck in winter and highlights the need to severely restrict grazing of domestic horses on the range of the Przewalski’s horses. Khulan are less constrained by water and seem more flexible in their choice of diet or less successful in exploiting grass dominated habitats in winter due to human presence. Providing additional water sources could increase the competition between khulan and livestock, and should therefore be only done following careful consideration.

Concepts: Horse, Pasture, Livestock, Grazing, Equus, Equidae, Donkey, Przewalski's Horse

9

Megafaunas worldwide have been decimated during the late Quaternary. Many extirpated species were keystone species, and their loss likely has had large effects on ecosystems. Therefore, it is increasingly considered how megafaunas can be restored. The horse (Equus ferus) is highly relevant in this context as it was once extremely widespread and, despite severe range contraction, survives in the form of domestic, feral, and originally wild horses. Further, it is a functionally important species, notably due to its ability to graze coarse, abrasive grasses. Here, we used species distribution modelling to link locations of wild-living E. ferus populations to climate to estimate climatically suitable areas for wild-living E. ferus. These models were combined with habitat information and past and present distributions of equid species to identify areas suitable for rewilding with E. ferus. Mean temperature in the coldest quarter, precipitation in the coldest quarter, and precipitation in the driest quarter emerged as the best climatic predictors. The distribution models estimated the climate to be suitable in large parts of the Americas, Eurasia, Africa, and Australia and, combined with habitat mapping, revealed large areas to be suitable for rewilding with horses within its former range, including up to 1.5 million ha within five major rewilding areas in Europe. The widespread occurrence of suitable climates and habitats within E. ferus' former range together with its important functions cause it to be a key candidate for rewilding in large parts of the world. Successful re-establishment of wild-living horse populations will require handling the complexity of human-horse relations, for example, potential conflicts with ranchers and other agriculturalists or with other conservation aims, perception as a non-native invasive species in some regions, and coverage by legislation for domestic animals.

Concepts: Climate, Ecosystem, Climate change, Horse, Extinction, Invasive species, Wild horse, Przewalski's Horse

7

The mammal gut microbiome, which includes host microbes and their respective genes, is now recognized as an essential second genome that provides critical functions to the host. In humans, studies have revealed that lifestyle strongly influences the composition and diversity of the gastrointestinal microbiome. We hypothesized that these trends in humans may be paralleled in mammals subjected to anthropogenic forces such as domestication and captivity, in which diets and natural life histories are often greatly modified. We investigated fecal microbiomes of Przewalski’s horse (PH; Equus ferus przewalskii), the only horses alive today not successfully domesticated by humans, and herded, domestic horse (E. f. caballus) living in adjacent natural grasslands. We discovered PH fecal microbiomes hosted a distinct and more diverse community of bacteria compared to domestic horses, which is likely partly explained by different plant diets as revealed by trnL maker data. Within the PH population, four individuals were born in captivity in European zoos and hosted a strikingly low diversity of fecal microbiota compared to individuals born in natural reserves in France and Mongolia. These results suggest that anthropogenic forces can dramatically reshape equid gastrointestinal microbiomes, which has broader implications for the conservation management of endangered mammals.

Concepts: Mammal, Horse, Wild horse, Equus, Donkey, Domestication of the horse, Przewalski's Horse, Tarpan

7

Przewalski’s horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts. The current population is still endangered, with just 2,109 individuals, one-quarter of which are in Chinese and Mongolian reintroduction reserves [1]. These horses descend from a founding population of 12 wild-caught PHs and possibly up to four domesticated individuals [2-4]. With a stocky build, an erect mane, and stripped and short legs, they are phenotypically and behaviorally distinct from domesticated horses (DHs, Equus caballus). Here, we sequenced the complete genomes of 11 PHs, representing all founding lineages, and five historical specimens dated to 1878-1929 CE, including the Holotype. These were compared to the hitherto-most-extensive genome dataset characterized for horses, comprising 21 new genomes. We found that loci showing the most genetic differentiation with DHs were enriched in genes involved in metabolism, cardiac disorders, muscle contraction, reproduction, behavior, and signaling pathways. We also show that DH and PH populations split ∼45,000 years ago and have remained connected by gene-flow thereafter. Finally, we monitor the genomic impact of ∼110 years of captivity, revealing reduced heterozygosity, increased inbreeding, and variable introgression of domestic alleles, ranging from non-detectable to as much as 31.1%. This, together with the identification of ancestry informative markers and corrections to the International Studbook, establishes a framework for evaluating the persistence of genetic variation in future reintroduced populations.

Concepts: Gene, Genetics, Horse, Extinction, Wild horse, Domestication of the horse, Przewalski's Horse, Tarpan

6

Leadership is commonly invoked when accounting for the coordination of group movements in animals, yet it remains loosely defined. In parallel, there is increased evidence of the sharing of group decisions by animals on the move. How leadership integrates within this recent framework on collective decision-making is unclear. Here, we question the occurrence of leadership in horses, a species in which this concept is of prevalent use. The relevance of the three main definitions of leadership - departing first, walking in front travel position, and eliciting the joining of mates - was tested on the collective movements of two semi-free ranging groups of Przewalski horses (Equus ferus przewalskii). We did not find any leader capable of driving most group movements or recruiting mates more quickly than others. Several group members often displayed pre-departure behaviours at the same time, and the simultaneous departure of several individuals was common. We conclude that the decision-making process was shared by several group members a group movement (i.e., partially shared consensus) and that the leadership concept did not help to depict individual departure and leading behaviour across movements in both study groups. Rather, the different proxies of leadership produced conflicting information about individual contributions to group coordination. This study discusses the implications of these findings for the field of coordination and decision-making research.

Concepts: Decision making, Horse, Leadership, Wild horse, Equus, Przewalski's Horse, Tarpan